Introduction
Bromus (Poaceae) is a large genus of grasses that includes nearly 160 C3 species with wide geographic distribution (Acedo and Llamas Reference Acedo and Llamas2001). The genus contains annuals, biennials, and perennials either self- or cross-pollinated and adapted to a wide range of environmental conditions (Armstrong Reference Armstrong, Armstrong, Tsuchiya and Gupta1991). This genus is well known for its complex taxonomy (Acedo and Llamas Reference Acedo and Llamas1999) due to morphological variation, plasticity, and hybridization (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008). Polyploidy and hybridization have played a major role in the evolution of this genus, resulting in a diversity of species with a different number of chromosomes and genome sizes (Stebbins Reference Stebbins1981). The Bromus genus contains species with ploidy levels ranging from diploid (2n = 2x = 14) to duodecaploid (2n = 12x = 84) with the basic chromosome number x = 7 (Williams et al. Reference Williams, Stewart, Williamson and Kole2011).
Bromus spp. have been treated in multiple ways by taxonomists because of the complexity of this genus. Tzvelev (Reference Tzvelev1976) classified the species into five distinct genera: Eubromus, Bromus, Ceratochloa, Neobromus, and Bromopsis. Smith (Reference Smith1970) divided the species into six sections: Genea, Bromus, Ceratochloa, Neobromus, Nevskiella, and Pnigma. Stebbins (Reference Stebbins1981) took an intermediate position and distributed the species into seven subgenera: Festucaria, Ceratochloa, Stenobromus, Bromus, Neobromus, Nevskiella, and Boissiera. Smith’s classification based on “sections” has been the most used since its publication in 1970. The sections are differentiated morphologically according to the number of nerves in the glumes, spikelet shape, and lemma and awn morphology, in addition to karyotypes, genome relationships (chromosome pairing), ploidy levels, and serological differences (Williams et al. Reference Williams, Stewart, Williamson and Kole2011). Among the six sections, the major agricultural species are in the Ceratochloa (Bromus catharticus Vahl., Bromus sitchensis Trin.) and Pnigma (Bromus inermis Leyss.) sections, whereas several species in the Genea (Bromus tectorum L., Bromus sterilis L., Bromus rubens L., B. madritensis L., Bromus rigidus Roth [syn.: Bromus diandrus Roth ssp. diandrus]) and Bromus (Bromus japonicus Thunb. [syn.: Bromus arvensis L.], Bromus secalinus L., Bromus commutatus Schrad. [syn.: Bromus racemosus L.]) sections are troublesome weeds of both agricultural and nonagricultural systems (Williams et al. Reference Williams, Stewart, Williamson and Kole2011).
Weeds are the main limiting factor in agricultural systems, because they reduce crop yield and profitability (Ghersa and Roush Reference Ghersa and Roush1993; Patterson Reference Patterson1995; Swanton and Weise Reference Swanton and Weise1991). Herbicides are considered the most cost-effective available tool for achieving successful weed control (Heap Reference Heap1997; Pleasant et al. Reference Pleasant, Burt and Frisch1994). However, the continuous reliance on weed management programs based heavily on herbicides has selected numerous herbicide-resistant weeds (Holt Reference Holt1992; Moss and Rubin Reference Moss and Rubin1993; Powles and Howat Reference Powles and Howat1990), including Bromus spp. (Table 1).
Table 1. Herbicide-resistant Bromus spp. reported globally and reviewed in this study.
a Herbicide site of action (SOA): ACCase, acetyl-coenzyme A carboxylase (Group 1); ALS, acetolactate synthase (Group 2); EPSPS, 5-enolpyruvyl shikimate-3-phosphate synthase (Group 9); HPPD, 4-hydroxyphenylpyruvate dioxygenase (Group 27); PSII, photosystem II (Groups 5 and 7); VLCFA, very-long-chain fatty-acid (Group 15).
b Chemical family abbreviations: AOPP, aryloxyphenoxypropionate; BF, benzofurane; CHD, cyclohexanedione; GLY, glycine; IMI, imidazolinone; PU, phenylurea; PY, pyrazole; SU, sulfonylurea; TAZ, triazinone; TAZN, triazolinones; TP, triazolopyrimidine; TZ, triazine; UR, urea.
c Mechanisms: NA, not available; NTSR, non–target site resistance; TSR, target-site resistance.
Herbicide-resistance mechanisms in weed species fall into two categories: (1) resistance conferred by mutations in the herbicide target enzyme or gene amplification (target-site resistance [TSR]) and (2) resistance conferred by mechanisms not involving the target enzyme (non–target site resistance [NTSR]) (Délye et al. Reference Délye, Jasieniuk and Corre2013; Gaines et al. Reference Gaines, Duke, Morran, Rigon, Tranel, Küpper and Dayan2020). TSR is typically determined by monogenic traits (i.e., conferred by major alleles) (Délye et al. Reference Délye, Jasieniuk and Corre2013; Scarabel et al. Reference Scarabel, Pernin and Délye2015). Conversely, NTSR can be under monogenic or polygenic control (i.e., governed by multiple alleles) (Busi et al. Reference Busi, Neve and Powles2013; Scarabel et al. Reference Scarabel, Pernin and Délye2015). NTSR mechanisms can be the result of physiological and biochemical alterations such as reduced herbicide absorption and translocation, enhanced herbicide metabolism, and herbicide vacuolar sequestration (Jugulam and Shyam Reference Jugulam and Shyam2019; Yuan et al. Reference Yuan, Tranel and Stewart2007). NTSR is of particular concern, because it can confer resistance to herbicides from different chemical families across multiple sites of action (SOAs), including herbicides not commercially available (Ma et al. Reference Ma, Kaundun, Tranel, Riggins, McGinness, Hager, Hawkes, McIndie and Riechers2013; Petit et al. Reference Petit, Bay, Pernin and Délye2010; Preston Reference Preston2003), thus limiting the herbicide options for weed control.
The evolution of herbicide resistance in Bromus spp. is of concern. Currently, there are 40 reports of herbicide resistance in the genus, including the diploids (2n = 2x = 14) B. japonicus, B. sterilis, and B. tectorum; the tetraploids (2n = 4x = 28) B. commutatus, B. madritensis, B. rubens, and B. secalinus; the hexaploids (2n = 6x = 42) B. catharticus and B. rigidus; and the octoploid (2n = 8x = 56) B. diandrus (Table 1). Herbicide resistance to six SOAs has been reported in Bromus spp.: acetyl-coenzyme A carboxylase (ACCase, Group 1), acetolactate synthase (ALS, Group 2), photosystem II (PSII, Groups 5 and 7), very-long-chain fatty-acid (VLCFA, Group 15), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS, Group 9), and 4-hydroxyphenylpyruvate dioxygenase (HPPD, Group 27) inhibitors. Cross-resistance is prevalent in Bromus spp., with 20 reports confirmed in six countries, including Australia, the Czech Republic, France, Germany, the United Kingdom, and the United States. Instances of cross-resistance include resistance to ACCase and ALS inhibitors (Ball et al. Reference Ball, Frost and Bennett2007; Davies et al. Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020; Kumar and Jha Reference Kumar and Jha2017; Owen et al. Reference Owen, Goggin and Powles2012, Reference Owen, Martinez and Powles2015; Ribeiro et al. Reference Ribeiro, Brunharo, Mallory-Smith, Walenta and Barroso2023; Sen et al. Reference Sen, Hamouzová, Mikulka, Bharati, Košnarová, Hamouz, Roy and Soukup2021). Multiple resistance is less common, with four cases confirmed in Bromus spp. In some regions, such as the United States Pacific Northwest, multiple resistance to two and four SOAs has been reported: the four SOAs were ACCase, ALS, PSII, and VLCFA (Mallory-Smith et al. Reference Mallory-Smith, Hendrickson and Mueller-Warrant1999; Park et al. Reference Park, Fandrich and Mallory-Smith2004; Park and Mallory-Smith Reference Park and Mallory-Smith2004, Reference Park and Mallory-Smith2005), and to two SOAs were ACCase and ALS inhibitors (Zuger and Burke Reference Zuger and Burke2020). The two other cases of multiple resistance were documented in Spain, with resistance to both ALS and EPSPS inhibitors (Escorial et al. Reference Escorial, Loureiro, Rodríguez-García and Chueca2011); and in China, with resistance to four SOAs: ACCase, ALS, PSII, and HPPD inhibitors (Lan et al. Reference Lan, Zhou, Lin, Cao, Wei, Huang, Li and Huang2022).
Because of the worldwide importance of the Bromus genus and the increasing cases of herbicide resistance, a comprehensive review that summarizes what is known about herbicide resistance in Bromus spp. is needed. Therefore, the objective of this review is to provide an update on the status of herbicide resistance in Bromus spp. globally and what is known about the resistance mechanisms. Additionally, relevant information, including the biology and genetics of Bromus spp., is provided to further the understanding of the resistance evolution and dispersal of the different species.
Bromus catharticus
Bromus catharticus, commonly known as prairie grass or rescue grass, is one of the major agricultural species of forage grass in the Bromus genus (Abbott et al. Reference Abbott, Filippini, Delfino and Pistorale2012). Native to South America, B. catharticus is an annual or short-lived perennial cool-season grass that has been introduced on a wide geographic scale, including Europe, Africa, Asia, Australia, New Zealand, and North America (Aulicino and Arturi Reference Aulicino and Arturi2002; Muzafar et al. Reference Muzafar, Khuroo, Mehraj, Hamid and Rashid2016; Williams et al. Reference Williams, Stewart, Williamson and Kole2011). This species is considered a valuable forage crop because of its high biomass production, fast growth rate during winter and spring, great adaptability, and ability to remain green after seed maturation (Sun et al. Reference Sun, Dong, Yang, Wu, Zhang, Zhang, Zhao, Xiong, Jia and Ma2021). In the Pampas of Argentina, B. catharticus is cultivated as a winter forage crop for grazing, but it can also behave as a weed in several winter crops such as wheat (Triticum aestivum L.), barley (Hordeum vulgare L.), and pea (Pisum sativum L.) (Poggio et al. Reference Poggio, Satorre and de la Fuente2004; Yanniccari et al. Reference Yanniccari, Vázquez-García, Gómez-Lobato, Rojano-Delgado, Alves and De Prado2021). Bromus catharticus typically germinates in midsummer and fall (Ahumada and Troiani Reference Ahumada and Troiani2016; Iroulart Reference Iroulart2020), when applications of glyphosate are extensively performed for weed control before to planting winter cereals such as wheat and barley (Vigna et al. Reference Vigna, Papa, Ponsa, Bedmar, Guevara, Rainero, Olea, Gigón, Istilart, López, Arguissain, Picapietra, Fernández, Leguizamón and Acciaresi2014). If not controlled preplanting, B. catharticus can cause yield losses of up to 70% in these crops (Iroulart Reference Iroulart2020).
Biology and Genetics
Bromus catharticus reproduces entirely by seeds, and its inflorescences consist of drooping panicles with spikelets that are strongly laterally compressed and attached to 2- to 4-cm-long pedicels (Auld and Medd Reference Auld and Medd1987). Lemmas have a short awn (<5 mm) arising right below the apex. Bromus catharticus can produce both cleistogamous (closed) and chasmogamous (open) flowers, but its reproduction is mainly through self-pollination, although outcrossing can occur (Gutierrez and Pensiero Reference Gutierrez and Pensiero1998; Naranjo Reference Naranjo1992; Rosso et al. Reference Rosso, Pagano, Rimieri and Ríos2009; Table 2). The outcrossing rate for this species was estimated to be 1.8% (Morant et al. Reference Morant, Pahlen, Cladera and Serrano1994). Flowering depends on flower morphology, photoperiod, and soil moisture (Ragonese and Marcó Reference Ragonese and Marcó1941, Reference Ragonese and Marcó1943). For instance, the chasmogamic flowering period typically happens at the beginning of spring, and the cleistogamic period at the end of spring and during the summer (Perez López Reference Perez López1975).
Table 2. Biology and genetics of Bromus spp. globally reviewed in this study.
a Nuclear DNA amount 1C values were obtained in the website: https://cvalues.science.kew.org/search.
b Genome size was estimated based on the conversion of nuclear 1C DNA amount in picograms to the numbers of base pairs suggested by Doležel et al. (Reference Doležel, Greilhuber and Suda2007): 1 pg DNA = 0.978 × 109 bp.
Bromus catharticus is a hexaploid species (2n = 6x = 42; AABBCC; 12.36-Gb genome size) in the Ceratochloa section (Stebbins and Tobgy Reference Stebbins and Tobgy1944; Table 2), with a nuclear DNA content of 12.64 pg (Klos et al. Reference Klos, Sliwinska, Kula, Golczyk, Grabowska-Joachimiak, Ilnicki, Szostek, Stewart and Joachimiak2009). This species has an allopolyploid origin that probably arose through hybridization between extinct diploid (2x) and tetraploid (4x) species (Stebbins Reference Stebbins1956).
Despite being predominantly self-pollinated, hybridization between B. catharticus and other Bromus spp. is possible (Table 3). Bromus catharticus can hybridize with Bromus bonariensis Parodi & J.A. Cámara, Bromus brevis Nees ex Steud. (syn.: B. catharticus), Bromus parodii Covas & Itria (Naranjo Reference Naranjo1992), Bromus carinatus Hook. & Arn. (Stebbins and Tobgy Reference Stebbins and Tobgy1944), and Bromus haenkeanus (J. Presl) Kunth (syn.: B. catharticus) (Hall Reference Hall1955). Bromus catharticus can produce fertile hybrids (≤7.9% pollen viability and ≤3.48% flowers with mature seeds) when crossed with B. brevis (7.9% pollen viability and 2.8% flowers with mature seeds), B. parodii (6.8% pollen viability and 4.81% flowers with mature seeds) (Naranjo Reference Naranjo1992), and B. haenkeanus (4% seed fertility) (Hall Reference Hall1955). In contrast, B. catharticus × B. bonariensis (2.4% pollen viability and 0% flowers with mature seeds) and B. catharticus × B. carinatus hybrids are sterile (Naranjo Reference Naranjo1992; Stebbins and Tobgy Reference Stebbins and Tobgy1944).
Table 3. Interspecific hybridization of Bromus spp. reviewed in this study.
a NR, not reported. The study only indicated compatibility between species.
Resistance in Bromus catharticus
Glyphosate-resistant B. catharticus was identified in 2017 in Argentina (Yanniccari et al. Reference Yanniccari, Vázquez-García, Gómez-Lobato, Rojano-Delgado, Alves and De Prado2021; Table 1). The resistant population was found in a fallow field that had been under wheat–soybean [Glycine max (L.) Merr.] and barley–soybean crop rotations for at least 8 yr with frequent use of glyphosate. This resistant population was 4-fold less sensitive to glyphosate compared with the susceptible population. No evidence of TSR or enhanced glyphosate metabolism was detected in the resistant population. Conversely, lower foliar retention of glyphosate (138.34 μl solution g−1 dry weight vs. 390.79 μl solution g−1 dry weight), reduced absorption (54.18% vs. 73.56%), and translocation (27.70% vs. 62.36%) of [14C]glyphosate from the labeled leaf were observed in this glyphosate-resistant population. As a consequence, the resistant plants accumulated a 4.1-fold lower concentration of [14C]glyphosate in the roots compared with the susceptible plants. Therefore, low foliar retention of glyphosate and reduced herbicide absorption and translocation were reported to be the major mechanisms endowing NTSR in B. catharticus. This is the only case of resistance reported in B. catharticus. Because of B. catharticus’s reproductive system and widespread occurrence and the number of sympatric, compatible species, the risk of transferring herbicide-resistance alleles from B. catharticus to other Bromus spp. exists and should be of concern. In the Pampas of Argentina, B. bonariensis, B. brevis, and B. parodii occur sympatrically with B. catharticus, and they are sexually compatible (Leofanti and Camadro Reference Leofanti and Camadro2017; Naranjo Reference Naranjo1992); therefore, hybridization under field conditions and spread of resistance alleles is possible.
Bromus commutatus
Bromus commutatus, known as meadow brome or hairy chess, is native to Europe and western Asia and has been introduced throughout North America (Pavlick Reference Pavlick1995; Williams et al. Reference Williams, Stewart, Williamson and Kole2011). In the United Kingdom, B. commutatus is a troublesome weed commonly found in field margins and headlands of winter cereal crops and rarely seen in spring crops (Cussans et al. Reference Cussans, Cooper, Davies and Thomas1994). This species has become more widespread and difficult to control in the United Kingdom because of the increased adoption of minimum tillage; restricted crop rotations, including mainly fall-sown crops; and limited effective herbicide options for control (Davies and Hull Reference Davies and Hull2018). Bromus commutatus can have winter or spring annual or biennial life cycles (Finnerty and Klingman Reference Finnerty and Klingman1962; Table 2). Integrating cultural and mechanical practices, including late sowing (beyond the conventional fall window), spring crop rotation, and stubble management using improved mechanical weeders, is a key strategy to control B. commutatus, reduce herbicide dependence, and consequently, reduce herbicide-resistance evolution (Clarke et al. Reference Clarke, Moss and Orson2000).
Biology and Genetics
Bromus commutatus is largely self-pollinated and only reproduces by seeds (Table 2). Bromus commutatus produces flowers on a panicle with ascending branches (12- to 25-cm long) containing pediceled spikelets (1.8- to 3.3-cm long; 8 to 11 flowered) with awns (8- to 11-mm long) (Bryson and DeFelice Reference Bryson and DeFelice2010). In the United Kingdom, seed is usually shed between May and October, and seedling emergence takes place between July and November (Bayer Crop Science UK 2022). Research has shown that B. commutatus seeds should be left on the soil surface for approximately 28 d before any tillage, because warm temperatures minimize seed dormancy (Clarke et al. Reference Clarke, Moss and Orson2000). Subsequently, the utilization of mechanical control methods such as plowing becomes more effective, resulting in less viable seed after burial.
Bromus commutatus is an allotetraploid species (2n = 4x = 28; 10.66-Gb genome size) belonging to the Bromus section (Table 2), with a nuclear DNA content of 10.90 pg (Bennett and Smith Reference Bennett and Smith1976). The allopolyploid origin of this species has not been reported in the literature.
Although B. commutatus is predominantly self-pollinated, hybridization between B. commutatus and other Bromus spp. can occur (Armstrong et al. Reference Armstrong, Fitzjohn, Newstrom, Wilton and Lee2005; Table 3). Bromus commutatus (4x) and Bromus racemosus (4x) are interfertile, and naturally occurring hybrids are produced (Smith Reference Smith1973). Hybrids of B. arvensis (2x) × B. commutatus (4x) and Bromus macrostachys Desf. (4x) × B. commutatus (4x) resulted in some chromosome pairing, suggesting a compatibility relationship between these genomes (Jahn Reference Jahn1959). Bromus mollis auct. Non L. (syn.: Bromus hordeaceus L. ssp. hordeaceus) (4x) and B. commutatus (4x) crossed readily, but F1 hybrid seeds did not germinate (Knowles Reference Knowles1944).
Resistance in Bromus commutatus
A case of cross-resistance to ALS-inhibiting herbicides was reported in B. commutatus in the United Kingdom with resistance to mesosulfuron-methyl + iodosulfuron-methyl-sodium and pyroxsulam (Davies et al. Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020; Table 1). This population was >16 times more resistant to mesosulfuron-methyl + iodosulfuron-methyl-sodium and pyroxsulam compared with the susceptible population. Molecular evidence suggested that cross-resistance to sulfonylurea (mesosulfuron-methyl + iodosulfuron-methyl-sodium) and triazolopyrimidine (pyroxsulam) chemical families in B. commutatus resulted from both TSR and NTSR mechanisms. The ALS gene sequence analysis revealed an amino acid substitution from tryptophan to leucine at position 154 (Trp-154-Leu). Additionally, enhanced levels of the glutathione transferase phi (F) class 1 enzyme, referred to as AmGSTF1, were detected in the resistant population compared with the susceptible population (Davies et al. Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020). This enzyme has a functional role in regulating NTSR. Based on the reports of sexual compatibility between B. commutatus and other Bromus spp., the transfer of resistance alleles from herbicide-resistant B. commutatus to other Bromus spp. is possible. In the United Kingdom, a survey of growers and agronomists reported the occurrence of multiple Bromus spp., including B. commutatus, B. diandrus, B. hordeaceus, B. secalinus, and B. sterilis, across cereal-growing areas (Davies and Hull Reference Davies and Hull2018). These species were present on 34,730 ha of cropland and were reported to occur in 39 of 168 fields surveyed. Although sexual compatibility among these species has not been documented in the literature, research on potential outcrossing among these species would be relevant, as they are locally distributed and co-occur.
Bromus diandrus
Bromus diandrus, known by the common names ripgut brome or great brome, is a winter annual species (Table 2) native to the Mediterranean region and widely introduced elsewhere in the world. This species is a highly competitive weed in cereal crops in different geographies including Europe, Asia, Africa, North America, and Oceania (Clapham et al. Reference Clapham, Tutin and Warburg1952; Kon and Blacklow Reference Kon and Blacklow1989). Previous research has shown that a B. diandrus infestation of 100 plants m−2 can cause a yield loss of 30% in wheat (Gill et al. Reference Gill, Poole and Holmes1987). Moreover, B. diandrus seed can contaminate harvested grain and cause injury to livestock if the awns become embedded in the animal’s nose or mouth when grazing (Kon and Blacklow Reference Kon, Blacklow, Groves, Shepherd and Richardson1995). The increased cropping frequency through minimum tillage and the lack of effective herbicide options for selective B. diandrus control have resulted in a significant increase in the importance of this species in cereal crops in southern Australia (Gill and Blacklow Reference Gill and Blacklow1985; Heenan et al. Reference Heenan, Taylor and Leys1990; Kon and Blacklow Reference Kon and Blacklow1988), Spain (Fernandez Garcia and García-Baudín Reference Fernandez García and García-Baudín1997), and the United Kingdom (Davies and Hull Reference Davies and Hull2018). This high incidence of B. diandrus in cereal crops under no-till systems may be associated with the germination behavior of this species, which increases the difficulty of its control (Kleemann and Gill Reference Kleemann and Gill2013). Bromus diandrus germination is characterized by two distinct flushes when soil moisture and temperature are not limiting (Del Monte and Dorado Reference Del Monte and Dorado2011). The first and main flush typically occurs in fall with the first rains, originating from superficially buried or shaded (by the field stubble) seeds. The second flush occurs in spring and comes from seeds that remain on the soil surface. In this second flush, the seeds are directly exposed to light, and germination is inhibited by light; hence, the dormancy is prolonged until seeds lose their negative photoblastism and germination can occur. Therefore, delayed B. diandrus establishment allows this species to escape preplanting weed control tactics and infest crops where its selective control is more difficult.
Biology and Genetics
Bromus diandrus produces loose and drooping panicles, 150- to 200-mm long, with long spikelet branches (Kon and Blacklow Reference Kon and Blacklow1988). The lemma of this species is short (≤1 mm) and rounded at the tips. Bromus diandrus plants are largely self-pollinated with outcrossing frequencies of less than 1% (Kon and Blacklow Reference Kon and Blacklow1990; Table 2). Chasmogamy in B. diandrus commonly occurs under favorable conditions such as high soil moisture (Kon and Blacklow Reference Kon and Blacklow1990). Under irrigated conditions, the anthers of B. diandrus in the chasmogamous florets (2- to 8-mm long) were longer than those in cleistogamous florets (<2 mm). In the same study, attempts at hybridization between B. diandrus × B. rigidus failed, and there was no evidence of naturally occurring hybrids. Thus, further research is needed to investigate pollen viability under different levels of soil moisture, temperature, relative humidity, and flowering synchrony, as well as potential hybridization between B. diandrus and other species.
Bromus diandrus is an allooctoploid species (2n = 8x = 56; 11.64-Gb genome size) classified into the Genea section (Table 2), with a nuclear DNA content of 11.90 pg (Bennett and Smith Reference Bennett and Smith1976). Bromus diandrus may have originated from the hexaploid B. rigidus (female genome donor) and the diploid B. sterilis (male genome donor), and the proposed genomic formula for this species is either AABBCCDD (disomic inheritance) or AAAABBCC (disomic and tetrasomic inheritance) (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008).
Resistance in Bromus diandrus
Bromus diandrus populations have evolved resistance to three herbicide groups: ACCase inhibitors, ALS inhibitors, and the EPSPS inhibitor (glyphosate) (Table 1). The evolution of cross-resistance to ALS- and ACCase-inhibiting herbicides has been widely documented in B. diandrus populations in Australia (Boutsalis and Preston Reference Boutsalis and Preston2006; Boutsalis et al. Reference Boutsalis, Preston and Gill2012; Owen et al. Reference Owen, Martinez and Powles2015) and the United Kingdom (Davies et al. Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020). Boutsalis and Preston (Reference Boutsalis and Preston2006) identified an ACCase-resistant population that exhibited high levels of resistance to fluazifop-P-butyl (resistance factor [RF] > 50) and haloxyfop-ethoxyethyl (RF = 24). Boutsalis et al. (Reference Boutsalis, Preston and Gill2012) found five ACCase-resistant populations with prevalent resistance to fluazifop-P-butyl (RF = 4 to 16) and quizalofop-P-ethyl (RF = 8 to 16), and to a lesser extent to clethodim (RF = 4 to 10) and haloxyfop-ethoxyethyl (RF = 3 to 7), and two ALS-resistant populations exhibiting moderate levels of resistance to mesosulfuron-methyl (RF = 4 to 5) and pyroxsulam (RF = 3 to 4). The population reported by Owen et al. (Reference Owen, Martinez and Powles2015) was cross-resistant to clethodim and fluazifop-P-butyl with >85% survival when treated with the labeled rate of these herbicides and survived two times the labeled rate of both herbicides. The ALS-resistant population reported in the United Kingdom was >5.8 and 2.7 times more resistant to mesosulfuron-methyl + iodosulfuron-methyl-sodium and pyroxsulam compared with the susceptible population, respectively (Davies et al. Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020). However, the mechanisms of resistance were not reported in the populations from Australia and the United Kingdom. Resistance to glyphosate was identified in two populations of B. diandrus in Australia (Malone et al. Reference Malone, Morran, Shirley, Boutsalis and Preston2016). These populations were 4.7- to 4.9-fold more resistant to glyphosate than the susceptible population. The mechanism of resistance in these two glyphosate-resistant B. diandrus populations was conferred by EPSPS gene amplification. These populations contained 10 to 36 additional copies of EPSPS compared with the susceptible population. Increased EPSPS expression was also observed in the resistant populations, but the levels were not correlated with the number of EPSPS copies. A case of multiple resistance in B. diandrus was documented in Spain with resistance to both glyphosate and sulfosulfuron, but the mechanism of resistance in this population was not elucidated (Escorial et al. Reference Escorial, Loureiro, Rodríguez-García and Chueca2011).
Bromus japonicus
Bromus japonicus, Japanese brome, is an indigenous Eurasian species commonly found along roadsides, in floodplain wetlands, and in agricultural areas, including wheat fields (Li Reference Li1998). This species is extensively dispersed in Asia, Australasia, Europe, Northern Africa, North America, and South America (Che et al. Reference Che, Yuan, Jin, Wang, Zhang, Hu, Wu and Tian2010). It is estimated that a B. japonicus infestation of 4 plants m−2 can result in 2.11% to 2.24% yield loss in wheat (Li et al. Reference Li, Du, Yuan, Guo, Li and Wang2016).
Bromus japonicus is a winter annual (Table 2) with seedlings typically emerging in September and October, flowering occurs in early May, and seed dispersal starts in early October (Baskin and Baskin Reference Baskin and Baskin1981). The optimum temperature for B. japonicus germination is between 25 and 30 C (Li et al. Reference Li, Tan, Li, Yuan, Du, Ma and Wang2015). The authors found that light and pH are not limiting factors in germination, except under highly acidic conditions (pH ≤ 4). Seedling emergence is relatively greater (98%) when seeds are left on the soil surface compared with seeds buried at a depth of 5 cm (7%). Additionally, the authors found that seeds are tolerant to osmotic potential and salinity, with germination occurring under a wide range of salt concentrations (20 to 320 mM).
Biology and Genetics
Bromus japonicus is exclusively self-pollinated (Oja et al. Reference Oja, Jaaska and Vislap2003; Table 2). It reproduces only by seeds, and a single plant can produce an average of 1,885 seeds that can be dispersed by water or wind due to their light weight (Wang Reference Wang1986). Bromus japonicus produces flowers on an open panicle, 17- to 30-cm long and 6- to 13-cm wide, with the lower branches drooping at maturity (Bryson and DeFelice Reference Bryson and DeFelice2010). Spikelets are 5 to 10 flowered, 2.0- to 3.2-cm long with awns. Glumes are 4.0- to 7.6-mm long, minutely scabrous, with the second glume longer than the first. The lemma is 7.2- to 9.1-mm long, scabrous, and tip bent-awned from between two teeth.
Bromus japonicus is a diploid species (2n = 2x = 14; 5.38-Gb genome size) in the Bromus section (Table 2), with a nuclear DNA content of 5.50 pg (Bennett and Smith Reference Bennett and Smith1976). Previous studies, including serological analysis (Smith Reference Smith1972), isozyme analysis (Oja et al. Reference Oja, Jaaska and Vislap2003), and DNA analyses (Ainouche and Bayer Reference Ainouche and Bayer1997; Ainouche et al. Reference Ainouche, Bayer, Gourret, Defontaine and Misset1999), showed that B. japonicus and Bromus squarrosus L. are closely related species. According to Oja and Paal (Reference Oja and Paal2007), these species can be reliably distinguished based on the lemma margin, where plants with conspicuously angled margins are identified as B. squarrosus.
Resistance in Bromus japonicus
Herbicide resistance in B. japonicus was first reported in the United States in 2007 (Heap Reference Heap2022) and in China in 2022 (Lan et al. Reference Lan, Zhou, Lin, Cao, Wei, Huang, Li and Huang2022; Table 1). In both cases, the reported populations were ALS resistant with broad-spectrum cross-resistance patterns. The population identified in China exhibited a 120-fold increase in flucarbazone-sodium resistance (Lan et al. Reference Lan, Zhou, Lin, Cao, Wei, Huang, Li and Huang2022). The DNA sequence analyses of the ALS gene revealed a single nucleotide substitution of CCC to TCC at codon 197, resulting in a Pro-197-Ser mutation. Additionally, the application of malathion + flucarbazone-sodium reduced the 50% growth inhibition rate (GR50) value of this population by 60%, suggesting a cytochrome P450 monooxygenase (P450)-mediated metabolic resistance. This population was cross-resistant to mesosulfuron-methyl and pyroxsulam, with ≥ 95% survival when treated with the labeled rate and two times the labeled rate of the herbicides. Multiple resistance to ACCase, PSII, and HPPD inhibitors was also observed in this population, with ≥90% survival when treated with the labeled rates of clodinafop-propargyl, isoproturon, and cypyrafluone.
Bromus madritensis
Bromus madritensis, known as compact brome, originated in the Mediterranean region (Oja Reference Oja2002b). This species is found in southern and western Europe, Northern Africa, the Middle East (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008), and North America (Oja Reference Oja2002b). Bromus madritensis grows in a variety of disturbed environments (Warembourg and Estelrich Reference Warembourg and Estelrich2001) and agricultural areas (Heap Reference Heap2022). Because of its close morphological similarity to B. rubens, there is controversy as to whether B. madritensis and B. rubens should be treated as subspecies (Sales Reference Sales1994) or as separate species (Oja Reference Oja2002b). Population genetics analysis suggested independent origins of B. madritensis and B. rubens (Oja and Jaaska Reference Oja and Jaaska1996). These species can also be differentiated based on their panicle and spikelet characteristics. Bromus madritensis typically has longer panicle branches and looser panicles, whereas B. rubens is distinguished by its brushlike condensed panicles (Oja Reference Oja2002b).
Biology and Genetics
Bromus madritensis has a winter annual life cycle and is predominantly self-pollinating (Table 2). Its panicles are longer (3 to 15 cm) than they are wide (2 to 6 cm) and less dense; panicle branches are 1 to 3 cm, ascending to spreading, never drooping, containing 1 or 2 spikelets (Hitchcock et al. Reference Hitchcock, Cronquist, Janish, Rumely, Shin and Porcino2018; Roché et al. Reference Roché, Brainerd, Wilson, Otting and Korfhage2019). Spikelets are 30 to 50 mm, longer than the panicle branches, with parallel sides or widening distally, and are moderately laterally compressed with 6 to 10 florets (Hitchcock et al. Reference Hitchcock, Cronquist, Janish, Rumely, Shin and Porcino2018; Roché et al. Reference Roché, Brainerd, Wilson, Otting and Korfhage2019). Glumes are pilose with lower glumes (5 to 10 mm, 1-veined) shorter than the upper ones (10 to 15 mm, 3-veined) (Hitchcock et al. Reference Hitchcock, Cronquist, Janish, Rumely, Shin and Porcino2018; Roché et al. Reference Roché, Brainerd, Wilson, Otting and Korfhage2019). Lemmas are 12- to 20-mm long with a linear-lanceolate shape, pubescent, and with awns (12 to 23 mm) (Hitchcock et al. Reference Hitchcock, Cronquist, Janish, Rumely, Shin and Porcino2018; Roché et al. Reference Roché, Brainerd, Wilson, Otting and Korfhage2019).
Bromus madritensis is a tetraploid species (2n = 4x = 28; 4.79-Gb genome size) in the Genea section (Table 2), with a nuclear DNA content of 4.90 pg (Bennett and Smith Reference Bennett and Smith1976). It has an allopolyploid origin that possibly resulted from the hybridization of the diploids Bromus fasciculatus C. Presl (maternal parent) and B. sterilis (paternal parent) (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008; Oja Reference Oja2002a; Oja and Jaaska Reference Oja and Jaaska1996).
Despite B. madritensis being predominantly self-pollinated, hybridization with other Bromus spp. has been reported (Table 3). Attempted hybridizations between B. mollis × B. madritensis showed compatibility between these two species; however, F1 hybrids were sterile (Knowles Reference Knowles1944). Compatibility with other species is unknown.
Resistance in Bromus madritensis
To date, there is only one report of herbicide resistance in B. madritensis (Vázquez-García et al. Reference Vázquez-García, Castro, Royo-Esnal, Palma-Bautista, Torra and De Prado2023; Table 1). In 2018, six glyphosate-resistant B. madritensis populations were identified in orchards and cereal fields in Spain (Vázquez-García et al. Reference Vázquez-García, Castro, Royo-Esnal, Palma-Bautista, Torra and De Prado2023). The resistant populations accumulated ≤600 μg g−1 shikimic acid and had RF > 4 based on 50% death rate (LD50) and GR50 values. Populations with higher RFs factors showed lower shikimic acid accumulation. The resistance mechanisms were not reported in the study.
Bromus rigidus
Bromus rigidus, rigid brome, is an indigenous Mediterranean species with a winter annual life cycle (Table 2) that has become a severe weed problem in cropping systems in Australia (Kon and Blacklow Reference Kon and Blacklow1990), New Zealand (Dastgheib et al. Reference Dastgheib, Rolston and Archie2003), and North America (Gleichsner and Appleby Reference Gleichsner and Appleby1989). In southern Australia, B. rigidus is commonly found in cropping areas with >250-mm annual rainfall and lighter, sandy soils (Kon and Blacklow Reference Kon, Blacklow, Groves, Shepherd and Richardson1995). In early vegetative growth stages, B. rigidus and B. diandrus are very similar morphologically, causing difficulties in identifying these species. Bromus rigidus differs from B. diandrus by having shorter and sparser hairs on the adaxial surface of the leaf blades (Kon and Blacklow Reference Kon and Blacklow1988). The germination behavior of these two species is also an important distinguishing feature. Bromus rigidus has longer seed dormancy compared with B. diandrus (Gill and Carstairs Reference Gill and Carstairs1988; Kleemann and Gill Reference Kleemann and Gill2006; Kon and Blacklow Reference Kon and Blacklow1988), and its seeds are more likely to persist in the soil from one growing season to the next (Kleemann and Gill Reference Kleemann and Gill2009). The longer seed dormancy observed in B. rigidus is related to inhibition factors in the embryo (Gill and Carstairs Reference Gill and Carstairs1988; Kleemann and Gill Reference Kleemann and Gill2006). Bromus rigidus germination is strongly inhibited by light exposure (Kleemann and Gill Reference Kleemann and Gill2006). Studies from Spain (Del Monte and Dorado Reference Del Monte and Dorado2011) and Australia (Kleeman and Gill Reference Kleemann and Gill2013) have shown that B. diandrus seems to be photosensitive, with seeds having longer dormancy when exposed to light. These findings differ from previous Australian studies, which reported that B. diandrus populations have low levels of seed dormancy (Cheam Reference Cheam1986; Gill and Blacklow Reference Gill and Blacklow1985; Gill and Carstairs Reference Gill and Carstairs1988; Harradine Reference Harradine1986).
Biology and Genetics
Bromus rigidus is a predominantly self-pollinated species (Table 2) with minimal outcrossing (Kon and Blacklow Reference Kon and Blacklow1990). The inflorescences of B. rigidus are erect and compact, 90- to 210-mm long, with short spikelet branches (Kon and Blacklow Reference Kon and Blacklow1988). The lemma calluses are elongated (≥1 mm), compressed, and pointed; the abscission scars are elliptical. Seed production in B. rigidus varies from 1,156 to 2,908 seeds per plant.
Bromus rigidus is an allohexaploid species (2n = 6x = 42; 8.41-Gb genome size) in the Genea section (Table 2), with a nuclear DNA content of 8.60 pg (Bennett and Smith Reference Bennett and Smith1976). This species is closely related to B. diandrus, and they share the same maternal parent. Based on a molecular phylogenetic study, there are at least three different genomes involved in the parentage of B. rigidus, including the diploids B. tectorum (T clade; TT), B. fasciculatus (F clade; FF), and an unidentified third ancestor (X clade; XX) (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008). It is unknown whether B. rigidus (XXFFTT) originated independently or from hybridization between a tetraploid ancestor (related to B. rubens) and an unidentified parent.
Previous research reported compatibility between B. mollis and B. rigidus (Knowles Reference Knowles1944; Table 3). In the same study, the cross between B. mollis × B. rigidus yielded a total of 10 seeds, but none germinated. Further research investigating the potential hybridization between B. rigidus and other Bromus spp. is needed.
Resistance in Bromus rigidus
Herbicide resistance to ACCase and ALS inhibitors was documented in B. rigidus populations in Australia, including single- and cross-resistance cases (Table 1). Because there are limited herbicide options for selective B. rigidus control in crops, the selection for resistance to these two herbicide SOAs is a loss for Australian growers. Owen et al. (Reference Owen, Goggin and Powles2012) identified six B. rigidus populations that were resistant to the ALS inhibitors sulfometuron-methyl (RF ≥ 3) and sulfosulfuron (RF ≥ 6) from Western Australia. Similar findings were reported 3 yr later in the same region, showing that the continued selection in the field by the use of the ALS-inhibiting herbicides sulfometuron-methyl and sulfosulfuron resulted in 100% plant survival at the field rate (Owen et al. Reference Owen, Martinez and Powles2015). In both studies, resistance was reversed when the plants were treated with malathion, suggesting enhanced metabolism (NTSR) as mechanism of resistance. The ACCase resistance mechanisms and cross-resistance mechanisms for both ACCase and ALS were not elucidated.
A survey conducted in the Western Australian grain belt showed the presence of several Bromus spp. in this region, including B. diandrus, B. rigidus, and B. rubens (Owen et al. Reference Owen, Martinez and Powles2015). These species were present in 91 of 466 crop fields surveyed. Bromus diandrus (85%) occurrence was widespread in all agronomic regions of the Western Australian grain belt; B. rigidus (13%) occurred in the northern agricultural region; and B. rubens (2%) was confined to the drier areas of the eastern wheat belt. The overlap of Bromus spp. commonly occurs in this region, particularly between B. diandrus and B. rigidus. Moreover, the presence of herbicide-resistant Bromus spp. populations has been documented. Of the 91 Bromus spp. populations screened in this survey, 13% exhibited resistance to ALS-inhibiting herbicides, and only one population was resistant to ACCase-inhibiting herbicides. All ALS-resistant populations were identified as B. rigidus, and the ACCase-resistant population was identified as B. diandrus. Because of the overlap of these species in some agronomic regions of the Western Australian grain belt and the evolution of herbicide-resistant populations, research investigating the hybridization between these species and potential gene flow is warranted.
Bromus rubens
Bromus rubens, red brome, is a Mediterranean grass species with widespread occurrence. This species is found in Southern Africa, Australasia, Europe, North America, and South America (USDA-ARS 2022a). Bromus rubens thrives in a variety of disturbed and non-disturbed environments and relatively shallow soils and drier areas (Crampton Reference Crampton1968). In North America, B. rubens is a successful colonizer in the southwestern United States deserts (Salo Reference Salo2004, Reference Salo2005). Bromus rubens was introduced to the United States in 1980 and has since become dominant in areas of the Mojave (Beatley Reference Beatley1966; Hunter Reference Hunter1991), Sonoran (Burgess Reference Burgess1965; Burgess et al. Reference Burgess, Bowers and Turner1991), and Great Basin deserts (Tausch et al. Reference Tausch, Svejcar and Burkhardt1994). This species can also be found in cropland. In southern Spain, growers utilize B. rubens as a cover crop in perennial cropping systems, such as olive (Olea europaea L.) and almond (Prunus amygdalus Batsch) orchards; however, this species has also become a severe weed in these systems (Vázquez-García et al. Reference Vázquez-García, Castro, Cruz-Hipólito, Millan, Palma-Bautista and De Prado2021). In Australia, B. rubens is a competitive weed in cereal crops and is confined to the drier areas of the eastern wheat belt in Western Australia (Owen et al. Reference Owen, Martinez and Powles2015). This distinctive ability of B. rubens to adapt to different environments is driven by key strategies such as rapid growth rates, high propagule pressure, low soil-moisture requirements for germination, and positive responses to disturbance, including fire (Beatley Reference Beatley1966; Salo Reference Salo2004; Wu and Jain Reference Wu and Jain1979). The optimal temperature for B. rubens germination is 19 C, with a hydrothermal-time constant of 38.9 MPa C−1 and water potential of −1.35 MPa (Horn et al. Reference Horn, Nettles and Clair2015). Bromus rubens does not have a persistent soil seedbank (Forcella and Gill Reference Forcella and Gill1986; Pake and Venable Reference Pake and Venable1995), and seed viability is negatively impacted by burial depth and timing (Jurand et al. Reference Jurand, Abella and Suazo2013). A relatively small proportion of B. rubens seed retained viability for 2 yr, and viable seed proportions were significantly lower at 5- and 10-cm burial depths.
Biology and Genetics
Bromus rubens is a winter annual, highly self-pollinating species (Table 2) with outcrossing rates of less than 0.1% (Wu Reference Wu1974). Bromus rubens produces a dense and erect panicle (2- to 10-cm long by 2- to 5-cm wide), often reddish-brown; branches are 0.1 to 1 cm, ascending, never drooping, with 1 or 2 spikelets (Hitchcock et al. Reference Hitchcock, Cronquist, Janish, Rumely, Shin and Porcino2018; Roché et al. Reference Roché, Brainerd, Wilson, Otting and Korfhage2019). Spikelets are much longer than the panicle branches, ranging from 18 to 25 mm, densely crowded, subsessile, with parallel sides or widening distally, moderately laterally compressed, with 4 to 8 florets. Glumes are pilose; lower glumes and upper glumes are 5 to 8 mm and 8 to 12 mm in length, respectively. Lemmas are linear-lanceolate (10- to 15-mm long) and awned (12- to 23-mm long).
Bromus rubens is an allotetraploid (2n = 4x = 28; 4.79-Gb genome size) in the Genea section (Table 2), with a nuclear DNA content of 4.90 pg (Bennett and Smith Reference Bennett and Smith1976). Bromus rubens and B. madritensis are closely related species derived from same the maternal donor (B. fasciculatus) and different paternal species (B. tectorum, and B. sterilis, respectively) (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008; Oja Reference Oja2002a). Despite the low outcrossing rates, hybridization between B. rubens × B. mollis can occur, but F1 hybrids are sterile (Knowles Reference Knowles1944; Table 3). Further investigations into reproductive compatibility between B. rubens and other species are needed.
Resistance in Bromus rubens
Bromus rubens populations have evolved resistance to glyphosate (Table 1). The first case of glyphosate resistance in B. rubens was documented in a fallow field in Australia in 2014 (Heap Reference Heap2022; Table 1). In 2018, 17 B. rubens populations were confirmed to be glyphosate resistant in perennial crops including almonds, olives, and other orchards in southern Spain (Vázquez-García et al. Reference Vázquez-García, Castro, Cruz-Hipólito, Millan, Palma-Bautista and De Prado2021). The RF in these populations varied from 4.35 to 7.61 (based on GR50 values) compared with the susceptible population. The resistant populations had lower shikimic acid accumulation (1,200 to 1,700 μg g−1 fresh weight) compared with the three susceptible populations (300 to 700 μg g−1 fresh weight) when treated with glyphosate. No difference in glyphosate retention was detected between the resistant and susceptible populations in the foliar retention assays. Further investigations are needed to characterize the mechanisms of resistance in these populations.
Bromus secalinus
Bromus secalinus, also known as rye brome or cheat, is a native species to Eurasia that has spread widely into warm and temperate regions globally (Williams et al. Reference Williams, Stewart, Williamson and Kole2011). This species is found on all continents except Antarctica (USDA-ARS 2022b). Bromus secalinus invades open waste areas, dry grasslands, limestone glades, grassy meadows, abandoned fields, field margins, roadsides, and railway tracks (Zech-Matterne et al. Reference Zech-Matterne, Derreumaux, Pradat, Luccioni, Ruas and Toulemonde2021). In croplands, B. secalinus is a common weed in cereal fields, particularly winter wheat and winter rye (Secale cereale L.) (Koscelny et al. Reference Koscelny, Peeper, Solie and Solomon1990; Pytlarz and Gala-Czekaj Reference Pytlarz and Gala-Czekaj2022), and other crops such as alfalfa (Medicago sativa L.) (Pike and Stritzke Reference Pike and Stritzke1984). Bromus secalinus typically grows in more acidic and sandy soils, but it also grows in damp clay soils (Zech-Matterne et al. Reference Zech-Matterne, Derreumaux, Pradat, Luccioni, Ruas and Toulemonde2021). Bromus secalinus typically germinates in the fall and less frequently in spring (Adamczewski et al. Reference Adamczewski, Kaczmarek, Kierzek and Urban2015). Optimum germination in B. secalinus occurs at temperature variations of 20/30 C. Seedling emergence is 89% to 92% when seeds are left on the soil surface and completely inhibited when seeds are located at 10-cm depth. The B. secalinus soil seedbank is relatively short-lived (2 to 3 yr). Because of its similar phenology to wheat, B. secalinus typically ripens simultaneously with this crop and can be a major contaminant of wheat grain during harvesting (Stone et al. Reference Stone, Peeper and Solie2001). Cultural practices such as row spacing, seeding rate, and planting date are the foundation for B. secalinus control in winter wheat, as selective herbicide options are limited (Koscelny et al. Reference Koscelny, Peeper, Solie and Solomon1990, Reference Koscelny, Peeper, Solie and Solomon1991).
Biology and Genetics
Bromus secalinus is a self-pollinated species and has an annual or biennial life cycle (Table 2). This species reproduces exclusively by seed, and a single plant can produce from 8,000 to 16,000 seeds (Adamczewski et al. Reference Adamczewski, Kaczmarek, Kierzek and Urban2015). The inflorescence of B. secalinus consists of an erect, loose, or contracted panicle, ranging from 5- to 23-cm long (Bryson and DeFelice Reference Bryson and DeFelice2010). The spikelets are 17- to 21-mm long, with 4 to 7 florets and pediceled. The first glume is 3- to 5-veined and is shorter in length (4 to 6 mm) than the second glume (6 to 8 mm). The lemma is 6- to 9-mm long with apical teeth, and the awn ranges from 1.5- to 9-mm long.
Bromus secalinus is an allotetraploid (2n = 4x = 28; 13.69-Gb genome size) in the Bromus section (Table 2), with a nuclear DNA content of 14.00 pg (Bennett and Smith Reference Bennett and Smith1976). Hybridization between B. secalinus and other Bromus spp. is not common but can occur (Table 3). Hybrids of B. arvensis (2x) × B. secalinus (4x) showed some chromosome pairing, indicating a relationship between the genome of these two species (Jahn Reference Jahn1959).
Resistance in Bromus secalinus
There are currently three confirmed cases of herbicide-resistant B. secalinus populations (Table 1). Two populations were identified in the United States in 2007 and 2009, respectively (Heap Reference Heap2022), and one population was documented in the United Kingdom in 2020 (Davies et al. Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020). All populations are resistant to ALS-inhibiting herbicides. Both resistant populations reported in the United States had broad cross-resistance patterns including all four ALS herbicide chemical families, imidazolinone, triazolopyrimidine, triazolinones, and sulfonylurea. The population identified in the United Kingdom was resistant to the sulfonylurea herbicide mesosulfuron + iodosulfuron-methyl-sodium (Davies et al. Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020). This population was 3.9-fold less sensitive to mesosulfuron + iodosulfuron-methyl-sodium compared with the susceptible population. The mechanisms of resistance in these populations were not reported.
Bromus sterilis
Bromus sterilis, commonly known as barren brome or poverty brome, is an annual or biennial grass species that originated in the Mediterranean and southwestern Asian region (Williams et al. Reference Williams, Stewart, Williamson and Kole2011; Table 2) and has been introduced into several countries in Australasia, North America, and South America (USDA-ARS 2023a). It naturally occurs in field margins and waste ground areas and has become a troublesome weed in cropland (Green et al. Reference Green, Barker, Marshall, Froud-Williams, Peters, Arnold, Dawson and Karp2001). This species is a particular problem in cereal crops because of the increased adoption of minimum tillage and limited herbicide options for its control. Lack of B. sterilis control can result in yield losses ranging from 30% to 60% in winter wheat (Gehring et al. Reference Gehring, Thyssen and Festner2006).
Bromus sterilis typically germinates in early fall with winter cereals and its germination can occur within a broad range of temperatures varying from 5 to 35 C (Žd’árková et al. Reference Žd’árková, Hamouzová, Holec, Janků and Soukup2014). The optimum temperature for its germination is between 20 and 30 C (95% to 100%) and germination is greater in the dark than in the light regardless of temperature. The primary dormancy of B. sterilis is typically short and lasts about a month. Previous research showed that light induces dormancy in B. sterilis (Peters et al. Reference Peters, Atkins and Brain2000; Pollard Reference Pollard1982). Seedling emergence is marginally greater when seeds are buried at a 2-cm depth (58.5%) than when they are left on the soil surface (53%) (Žd’árková et al. Reference Žd’árková, Hamouzová, Holec, Janků and Soukup2014). Bromus sterilis seeds retain short viability in the soil (<2 yr), suggesting a short-lived soil seedbank (Davies et al. Reference Davies, Hull, Moss and Neve2019; Žd’árková et al. Reference Žd’árková, Hamouzová, Holec, Janků and Soukup2014).
Biology and Genetics
Bromus sterilis is predominantly self-pollinated with low levels of outcrossing occurring occasionally (Green et al. Reference Green, Barker, Marshall, Froud-Williams, Peters, Arnold, Dawson and Karp2001). The inflorescences of B. sterilis are open and nodding (10- to 20-cm long by 5- to 12-cm wide) with spreading branches typically longer than the spikelets (Meyers et al. Reference Meyers, Jaster, Mitchell and Hardison2015). It has 1 or 2 spikelets (20 to 35 mm), moderately laterally compressed, containing 5 to 9 florets. Glumes are smooth or scabrous; lower glumes (8 to 10 mm; 1- to 3-veined) are shorter than upper glumes (12 to 15 mm; 3- to 5-veined). Lemmas are 14 to 20 mm, narrowly lanceolate, pubescent, and 7- to 9-veined. Lemma awns are straight and range from 15 to 30 mm in length.
Bromus sterilis is a diploid (2n = 2x = 14; 2.91-Gb genome size) species in the Genea section (Table 2), with a nuclear DNA content of 2.98 pg (Pustahija et al. Reference Pustahija, Brown, Bogunic, Bašic, Muratovic, Ollier, Hidalgo, Bourge, Stevanovic and Sijak-Yakovev2013). This species is closely related to B. tectorum based on chloroplast DNA sequences (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008). Evidence in the literature suggests possible hybridization between B. sterilis and other Bromus spp. (Table 3). Based on isoenzyme analysis, B. sterilis (male parent) and B. fasciculatus (female parent) are the most plausible progenitors of B. madritensis (Oja Reference Oja2002a).
Resistance in Bromus sterilis
Herbicide resistance in B. sterilis has been reported in four countries, including the Czech Republic, France, Germany, and the United Kingdom (Table 1). Resistant B. sterilis populations were identified in cereals including wheat, postharvest stubble, and rapeseed/canola (Brassica napus L.) (Table 1). Resistance has been reported for ACCase inhibitors, ALS inhibitors, and for the EPSPS inhibitor glyphosate. An ACCase inhibitor–resistant B. sterilis population was documented in Germany and was cross-resistant to cycloxydim (cyclohexanedione [CHD]) and propaquizafop (aryloxyphenoxypropionate [AOPP]) (Table 1). Cases of cross-resistance to two and three ALS chemical families have been documented in resistant B. sterilis populations in the Czech Republic, France, and the United Kingdom. An ALS-resistant B. sterilis population found in a wheat field in the Czech Republic was 288 times less sensitive to pyroxsulam than a susceptible population and was cross-resistant to propoxycarbazone-sodium (RF = 575) and sulfometuron-methyl (RF = 88). The resistance mechanisms in this population were associated with overexpression of the ALS gene (almost 2-fold overexpression; TSR) and enhanced metabolism via P450 enzymes (NTSR) (Sen et al. Reference Sen, Hamouzová, Mikulka, Bharati, Košnarová, Hamouz, Roy and Soukup2021). In the United Kingdom, Davies et al. (Reference Davies, Onkokesung, Brazier-Hicks, Edward and Moss2020) reported B. sterilis populations with reduced sensitivity to the ALS inhibitors mesosulfuron + iodosulfuron-methyl-sodium (RF = 3.5 to 8.3) and pyroxsulam (RF = 2.9 to 16). Enhanced levels of AmGSTF1 proteins were observed in the resistant populations, suggesting the presence of an NTSR mechanism. Glyphosate-resistant B. sterilis populations were identified in postharvest stubble in the United Kingdom (Davies et al. Reference Davies, Hull, Moss and Neve2019). The effective rate to control 50% (ED50) of these resistant B. sterilis populations ranged from 420 to 810 g ha−1, resulting in an RF of 1.6 to 4.5. The mechanisms of resistance were not reported.
Bromus tectorum
Bromus tectorum, commonly known as downy brome or cheatgrass, is a native species from the Mediterranean and southwest Asian region (Williams et al. Reference Williams, Stewart, Williamson and Kole2011). Bromus tectorum has been introduced to northern Europe, North America, Japan, South Africa, Australia, New Zealand, South America, and in single localities in Iceland and Greenland (Mitich Reference Mitich1999; USDA-ARS 2023b). Genetic evidence suggests that B. tectorum’s introduction into North America occurred independently multiple times on both coasts (Bartlett et al. Reference Bartlett, Novak and Mack2002; Novak and Mack Reference Novak and Mack1993). The soil used as ballast in ships sailing from Eurasia into North America was probably one of the main carriers of B. tectorum seeds (Mitich Reference Mitich1999). The first report of B. tectorum in the United States was in Pennsylvania in 1790 (Muhlenberg Reference Muhlenberg1793). By the end of the 19th century, B. tectorum had expanded throughout the western United States (Mack Reference Mack1981). Bromus tectorum thrives in a variety of non-crop disturbed and cultivated habitats and can occur in locations with annual rainfall ranging from 150 to 560 mm, including different soil types, and at elevations as high as 2,700 m (Hull and Pechanec Reference Hull and Pechanec1947). In the United States Pacific Northwest, B. tectorum is a problematic weed in dryland winter wheat fields (Rydrych Reference Rydrych1974). In eastern Washington, fewer than 54 B. tectorum plants m−2 reduced wheat yields by 28% on a field with very fine sandy loam soil that received annual precipitation of 250 mm (Rydrych and Muzik Reference Rydrych and Muzik1968). On a field with silt loam soil that received annual precipitation of 550 mm, more than 538 B. tectorum plants m−2 reduced winter wheat yields by 92% (Rydrych and Muzik Reference Rydrych and Muzik1968). Bromus tectorum is a winter annual that typically germinates in the fall shortly after the first onset of rains (Morrow and Stahlman Reference Morrow and Stahlman1984). If fall moisture is limiting, B. tectorum can germinate in the spring (Hulbert Reference Hulbert1955; Stewart and Hull Reference Stewart and Hull1949). Freshly produced seeds become dormant after dispersal in early summer and lose dormancy through afterripening (Allen and Meyer Reference Allen and Meyer2002). Nondormant seeds can germinate at temperatures ranging from 5 to 30 C (Evans and Young Reference Evans and Young1984). Seedling emergence is greater at 2- (100%) than at 4- (93%) or 6-cm depths (14%) (Hulbert Reference Hulbert1955). Most B. tectorum seeds germinate (96% to 99%) in the first year after entering the soil seedbank (Burnside et al. Reference Burnside, Wilson, Weisberg and Hubbard1996), with few persisting longer than 2 yr (Haferkamp et al. Reference Haferkamp, Heitschmidt, Elaine, MacNeil and Karl2001; Smith et al. Reference Smith, Meyer and Anderson2008). In a winter wheat–summer fallow rotation, B. tectorum seed viability was less than 2% by the third year (Rydrych Reference Rydrych1974).
Biology and Genetics
Bromus tectorum reproduces solely by seeds (Hulbert Reference Hulbert1955). It produces loose and drooping panicles between 4- to 18-cm long with a purplish cast when mature (Bryson and DeFelice Reference Bryson and DeFelice2010). Spikelets are 1.9- to 2.3-cm long including awns and contain 4 to 8 flowers. Glumes are pubescent or glabrous; the first glume ranges from 4- to 9-mm long (1-veined) and the second glume ranges from 7- to 13-mm long (3- to 5-veined). The lemma is 9- to 12-mm long, pubescent, with an awn of 10- to 18-mm long. The palea (1.2 to 2.1 mm) is shorter than the lemma and ciliates on nerves.
Bromus tectorum is a diploid species (2n = 2x = 14; 3.23-Gb genome size) in the Genea section (Table 2), with a nuclear DNA content of 3.30 pg (Bennett and Smith Reference Bennett and Smith1976). Bromus tectorum is predominantly self-pollinated, but outcrossing can occur (Ashley and Longland Reference Ashley and Longland2007; Meyer et al. Reference Meyer, Ghimire, Decker, Merrill and Coleman2013; Novak and Mack Reference Novak and Mack2016). The estimated outcrossing rate for four wild B. tectorum populations from the western United States ranged from 0.27% to 1.33% (Meyer et al. Reference Meyer, Ghimire, Decker, Merrill and Coleman2013). Significant levels of genotypic and phenotypic variations have been detected in B. tectorum populations, which are major drivers of B. tectorum successful invasion across different environments (Ashley and Longland Reference Ashley and Longland2007). Based on chloroplast data, B. tectorum (paternal parent), and B. fasciculatus (maternal parent) were the progenitors of B. rubens (Fortune et al. Reference Fortune, Pourtau, Viron and Ainouche2008). Therefore, interspecific hybridization between B. tectorum and other Bromus spp. is possible (Table 3).
Resistance in Bromus tectorum
Bromus tectorum populations have evolved resistance to ACCase-, ALS-, and PSII-inhibiting herbicides, and to the EPSPS inhibitor glyphosate (Table 1). The first recorded case of herbicide resistance in B. tectorum was an atrazine-resistant population in a cornfield in France in 1981 (Table 1). In Spain, B. tectorum populations resistant to PSII inhibitors were found in an olive orchard (Menendez et al. Reference Menendez, Gonzalez-Gutierrez and De Prado2007) and wheat fields (Menendez et al. Reference Menendez, Bastida and De Prado2006). The resistant population (ED50 = 7.3 kg ai ha−1) identified in simazine-treated olive groves was 73-fold less sensitive to simazine compared with a susceptible population (ED50 = 0.1 kg ai ha−1) (Menendez et al. Reference Menendez, Gonzalez-Gutierrez and De Prado2007). Hill reaction assays showed the chloroplasts of the resistant population were >300 times less sensitive to simazine than the susceptible population, suggesting a target-site mutation (likely due to a mutation of the chloroplast psbA gene that encodes the D1 protein) as the molecular basis for resistance to simazine in this population (Menendez et al. Reference Menendez, Gonzalez-Gutierrez and De Prado2007). The resistant population reported in a wheat field required 7.4 kg ai ha−1 of chlortoluron to reduce growth by 50%, which was 3.4 times the rate required for the susceptible population (Menendez et al. Reference Menendez, Bastida and De Prado2006). Molecular investigations showed that chlortoluron metabolism in the resistant population decreased by 20% when treated with the P450 inhibitor 1-ABT, suggesting a non–target site based resistance via P450–mediated metabolism.
In the United States Pacific Northwest, resistance in B. tectorum is of increasing concern in grass seed production systems and dryland wheat-based cropping systems, where cross- or multiple-herbicide resistance is extensive (Table 1). In 1997, an ALS-resistant B. tectorum population was identified in Madras, OR, in Kentucky bluegrass (Poa pratensis L.) experimental plots (Mallory-Smith et al. Reference Mallory-Smith, Hendrickson and Mueller-Warrant1999). This population was cross-resistant to three ALS chemical families, including sulfonylurea (primisulfuron-methyl and sulfosulfuron), triazolinones (propoxycarbazone-sodium), and imidazolinone (imazamox) (Park and Mallory-Smith Reference Park and Mallory-Smith2004). There was a variation in the levels of resistance (based on GR50 values) for primisulfuron-methyl (RF = 18), sulfosulfuron (RF = 9), propoxycarbazone-sodium (RF = 40), and imazamox (RF = 14). The resistance mechanism in this population was related to enhanced metabolism via P450 enzymes (Park et al. Reference Park, Fandrich and Mallory-Smith2004). When [14C]propoxycarbazone-sodium was applied with 1-aminobenzotriazole (1-ABTP; P450 inhibitor), metabolism decreased by 20% at 12 h after treatment (Park et al. Reference Park, Fandrich and Mallory-Smith2004). ALS gene sequencing did not detect any mutation in this population (Park and Mallory-Smith Reference Park and Mallory-Smith2004). Further investigations revealed that this population was multiple resistant to clethodim (RF = 2.3) and fluazifop-P-butyl (RF = 1.9) (ACCase inhibitors); atrazine (RF > 14), terbacil (RF = 4.6), metribuzin (RF > 20), and diuron (RF = 3.1) (PSII inhibitors); and ethofumesate (RF = 4.2) (VLCFA inhibitor) (Park and Mallory-Smith Reference Park and Mallory-Smith2005). DNA sequence analysis of the psbA gene, the target site of PSII inhibitors, revealed a single amino acid substitution from serine (AGT) to glycine (GGT) at amino acid 264 in the D1 protein, indicating that resistance to the PSII inhibitors atrazine and metribuzin was due to a target-site mutation (Park and Mallory-Smith Reference Park and Mallory-Smith2005). The mechanisms of resistance to clethodim, fluazifop-P-butyl, and ethofumesate were not investigated. In 1998, another ALS-resistant B. tectorum population was found in a Kentucky bluegrass field in Oregon (Park and Mallory-Smith Reference Park and Mallory-Smith2004). This population was cross-resistant to two ALS chemical families, sulfonylurea (primisulfuron-methyl and sulfosulfuron), and triazolinones (propoxycarbazone-sodium) (Park and Mallory-Smith Reference Park and Mallory-Smith2004). The level of resistance calculated by the estimated GR50 values showed that this population was 317-, 263-, and 235-fold more resistant than the susceptible population to primisulfuron-methyl, sulfosulfuron, and propoxycarbazone-sodium, respectively. Resistance in this population was conferred by a single-nucleotide polymorphism (C to T) at amino acid position 197, resulting in a Pro-197-Ser substitution (Park and Mallory-Smith Reference Park and Mallory-Smith2004).
Kumar and Jha (Reference Kumar and Jha2017) identified an ALS-resistant B. tectorum population in an imidazoline-resistant wheat field in Montana, USA, with high-level resistance (RF = 110.1) to imazamox and low to moderate levels of cross-resistance to pyroxsulam (RF = 4.6) and propoxycarbazone (RF = 13.9). A target-site Ser-653-Asn mutation was detected in this population. In Washington, among 50 B. tectorum populations tested for resistance, 2% were multiple resistant to ACCase and ALS inhibitors, 52% were cross-resistant to multiple chemical families of ALS inhibitors, and 20% were resistant to a single chemical family of ALS-inhibiting herbicides (Zuger and Burke Reference Zuger and Burke2020). Additionally, three glyphosate-resistant B. tectorum populations (RF = 88 to 165) were confirmed but did not have resistance to any other herbicide SOA (Zuger and Burke Reference Zuger and Burke2020). Resistance to ALS inhibitors is also prevalent in B. tectorum populations in dryland winter wheat fields in Oregon, with cases of cross-resistance ranging from two to four ALS chemical families (Ribeiro et al. Reference Ribeiro, Brunharo, Mallory-Smith, Walenta and Barroso2023, unpublished data. Bromus tectorum populations cross-resistant to ACCase inhibitors were reported in fine fescue (Festuca L. spp.) fields in Oregon (Ball et al. Reference Ball, Frost and Bennett2007; Ribeiro et al. Reference Ribeiro, Brunharo, Mallory-Smith, Walenta and Barroso2023). In 2005, Ball et al. (Reference Ball, Frost and Bennett2007) identified an ACCase-resistant B. tectorum population in a creeping red fescue (Festuca rubra L. ssp. rubra Gaudin) seed production field in Oregon. The population exhibited high levels of resistance to fluazifop-P-butyl (RF > 16) and sethoxydim (RF > 23) and low levels of resistance to clethodim (RF > 2) and quizalofop-P-ethyl (RF > 3). Fifteen years later, nine more ACCase-resistant B. tectorum populations were found in fine fescue seed production fields in the same area (Ribeiro et al. Reference Ribeiro, Brunharo, Mallory-Smith, Walenta and Barroso2023). The levels of resistance varied among the populations for clethodim (RF = 5.1 to 14.5), sethoxydim (RF = 18.7 to 44.7), fluazifop-P-butyl (RF = 3.1 to 40.3), and quizalofop-P-ethyl (RF = 14.5 to 36). The ACCase sequence analysis indicated that the Ile-2041-Thr and Gly-2096-Ala mutations were the molecular basis of resistance to the ACCase-inhibiting herbicides in these populations. In 2021, a glyphosate-resistant B. tectorum population was documented in a rapeseed/canola field in Alberta, Canada (Geddes and Pittman Reference Geddes and Pittman2022). This population exhibited 8.3- to 9.5-fold resistance to glyphosate compared with two susceptible populations. The mechanism of resistance in this population was not elucidated. This population was the first glyphosate-resistant grass weed species confirmed in Canada.
In the United States, B. tectorum and other species such as B. commutatus, B. japonicus, B. secalinus, B. sterilis, and B. diandrus can occur in several agricultural systems, including wheat, alfalfa, and grass seed production fields (Finnerty and Klingman Reference Finnerty and Klingman1962; Koscelny et al. Reference Koscelny, Peeper, Solie and Solomon1990, Reference Koscelny, Peeper, Solie and Solomon1991). The presence of multiple Bromus spp. in the same field, particularly species with sexual compatibility, plays a key role in hybrid speciation as well as the spread of resistance alleles. Research on the risk of gene flow between herbicide-resistant and herbicide-susceptible populations is scarce. Therefore, further investigations into the risk of transferring herbicide-resistance alleles from B. tectorum to susceptible plants are needed, as outcrossing can occur.
Summary and Research Needs
Herbicide resistance in Bromus spp. is a global issue. Cases of resistance have been confirmed in B. japonicus, B. sterilis, B. tectorum, B. commutatus, B. madritensis, B. rubens, B. secalinus, B. catharticus, B. rigidus, and B. diandrus. Bromus spp. populations have evolved resistance to six known herbicide SOAs, ACCase (Group 1), ALS (Group 2), PSII (Groups 5 and 7), VLCFA (Group 15), EPSPS (Group 9), and HPPD (Group 27). Several mechanisms of resistance have been reported in Bromus spp., including TSR, NTSR, and combinations of both. The mechanisms of resistance in many Bromus spp. populations still need to be investigated. Knowledge about the mechanism of resistance and its genetic basis is important for designing suitable management strategies to address resistance management. High-throughput, rapid genetic assays have been developed for herbicide-resistance detection (Kersten et al. Reference Kersten, Rabanal, Herrmann, Hess, Kronenberg, Schmid and Weigel2023), and their deployment will help improve the development of weed management plans to ensure the proper chemistry is chosen. Knowledge of resistance mechanisms is particularly important for populations exhibiting NTSR, because this type of resistance mechanism can be unpredictable. Most studies tested Bromus spp. populations against a short list of herbicides. Therefore, it is possible that some of the populations are also resistant to other chemistries.
Bromus spp. are predominantly self-pollinated with low outcrossing rates (≤1.8%) occurring in some species. The outcrossing rate in some Bromus spp. has not been reported, although the literature indicates that sexual compatibility among species exists. Information on the hybridization of Bromus spp. is very limited and needs further investigation. Furthermore, environmental conditions can impact the outcrossing rates of other weed species, with increased temperatures enhancing the outcrossing rate (Matzrafi et al. Reference Matzrafi, Preston and Brunharo2020), and more information is needed for Bromus spp. in a climate change scenario. The transfer of herbicide-resistance alleles via pollen-mediated gene flow cannot be ruled out, as outcrossing can occur at low rates in some Bromus spp. Most research on hybridization between Bromus spp. has been done within a controlled environment (e.g., greenhouse). However, hybridization needs to be studied under field conditions. Chances of hybridization may be much greater under field conditions, because the number of plants present is greater. In addition, more studies are necessary to further elucidate hybrid seed viability, as well as potential for heterosis, and competitive ability. Although most hybrids produced between Bromus spp. have been reported to be sterile, research on interspecific hybridization involving other self-pollinating species such as jointed goatgrass (Aegilops cylindrica Host) and wheat showed restoration of self-fertility in the second backcross between these species (Zemetra et al. Reference Zemetra, Hansen and Mallory-Smith1998). Thus, this assumption of sterility of hybrids between Bromus spp. can be incorrect and needs further investigation. Because Bromus spp. are typically highly self-pollinating, the geographic spread of herbicide resistance occurs primarily by natural (water and wind) and anthropogenic seed dispersal. Therefore, research on tactics to reduce seed-mediated gene flow in Bromus spp., including practices such as harvest weed seed destruction, would be beneficial.
Although herbicide resistance has been reported for most Bromus spp., the underlying genetic, molecular, and physiological mechanisms of many species remain unknown. Because of the parallel evolution of herbicide resistance in diverse continents, cropping systems, and ecotypes, the Bromus genus provides an invaluable opportunity to understand convergent evolution under herbicide selection pressure.
The ploidy levels in Bromus spp. range from diploid (2n = 2x = 14) to duodecaploid (2n = 12x = 84). Self-pollination and polyploidization are important traits responsible for the colonization and invasion success of plant species in a wide range of habitats (Orsucci et al. Reference Orsucci, Milesi, Hansen, Girodolle, Glémin and Lascoux2020). Self-pollination provides reproductive insurance, allowing a single plant to initiate an invasion (Kreiner et al. Reference Kreiner, Stinchcombe and Wright2018), while polyploidization confers partial sheltering from the negative effect of inbreeding, particularly by masking deleterious alleles (Beest et al. Reference Beest, Roux, Richardson, Brysting, Suda, Kubešová and Pyšek2012). However, the scientific literature is limited regarding the influence of ploidy on herbicide-resistance mechanisms. Therefore, more in-depth research is needed to comprehend the complexities of herbicide resistance and evolution in Bromus spp.
Acknowledgments
This research was possible thanks to funds received by the Oregon Wheat Commission and the Crop and Soil Science Department of the College of Agriculture Sciences of Oregon State University. No conflicts of interest have been declared.
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