The “Taxonomic Journey” of North American Echinochloa

In 1972, Gould et al. published a strikingly different classification of Echinochloa species of North America (seven classes) than those published by Hitchcock (Reference Hitchcock1920) and Wiegand (Reference Wiegand1921) some 50 yr earlier. In addition to Hitchcock’s and Wiegand’s classification, a few more conflicting taxonomic treatments of the Echinochloa complex and related taxa in North America were described or defined in the 1950s, 60s, and 70s. The status of native and introduced (adventive) taxa and the intraspecific categories have been the major sources of taxonomic disagreement. Hitchcock and Chase (Reference Hitchcock and Chase1950) and most authors who have published studies of the species have combined native and introduced taxa listed under barnyardgrass, whereas Gould et al. (Reference Gould, Ali and Fairbrothers1972), following the ideas published by Wiegand (Reference Wiegand1921), separate the native populations as rough barnyardgrass [Echinochloa muricata (P. Beauv.) Fernald]. Previously, many authors attempted to clarify the phylogenetic/taxonomic problems in Echinochloa using seed protein electrophoresis and isozyme analyses (Asins et al. Reference Asíns, Carretero, Busto, Carbonell and De Barreda1999; Gonzalez-Andres et al. Reference González-Andrés, Pita and Ortiz1996), and several other molecular tools available at that time (Aoki and Yamaguchi Reference Aoki and Yamaguchi2008; Danquah et al. Reference Danquah, Johnson, Riches, Arnold and Karp2002; Roy et al. Reference Roy, Simon and Lapointe2000; Tabacchi et al. Reference Tabacchi, Mantegazza and Ferrero2006). Recently, Wu et al. (Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022) have more accurately distinguished Echinochloa species and varieties by integrating morphological characteristics with multiple pieces of genomic evidence, including genome size, reads mapping rate, genome coverage, phylogeny, and population structure, providing remarkable insights into the evolutionary trajectory of Echinochloa species.

Barnyardgrass is native to Eurasia but is distributed worldwide, principally in a latitudinal zone from 50°N to 40°S (Michael Reference Michael2003). It is common as an agrestal and as a ruderal weed in more than 60 countries and three dozen different crops (Holm et al. Reference Holm, Pancho, Herberger and Plucknett1991) and is widespread in North America from southern Canada to Mexico, occurring on disturbed, moist, waste ground and as a serious weed of rice and other irrigated crops. Barnyardgrass is highly variable with respect to growth form (Smith et al. Reference Smith, Finchum and Seaman1977), flowering time, inflorescence architecture, anthocyanin pigmentation, and awn length. Several ecological and physiological biotypes varying in sensitivity to herbicides were reported from the northwestern United States in the 1960s (Roché and Muzik Reference Roché and Muzik1964). In North America, barnyardgrass is uniformly hexaploid, 2n = 6x = 54 (Gould et al. Reference Gould, Ali and Fairbrothers1972). Although the native species of North America, rough barnyardgrass, closely resembles barnyardgrass morphologically, they are genetically distant (Ruiz-Santaella et al. Reference Ruiz-Santaella, de Prado, Wagner, Fischer and Gerhards2006).

Also native to Eurasia, late watergrass (2n = 4x = 36), previously classified as E. crus-galli (L.) Beauv. var. oryzicola (Vasing.) Ohwi, E. oryzicola, E. oryzoides, E. phyllopogon, and E. macrocarpa is an obligate weed of rice fields occurring in rice-growing regions of Asia, Europe, Australia (Michael Reference Michael1983; Yabuno Reference Yabuno1966), and California (Barrett and Seaman Reference Barrett and Seaman1980). The introduction of late watergrass was primarily as a seed contaminant of rice seed stocks, as indicated by its collections right after the commencement of rice culture in California in 1912 through 1915 (Barrett and Seaman Reference Barrett and Seaman1980). Late watergrass established in monoculture Californian rice fields in the 1970s and is rarely found outside of the rice agroecosystem (Barrett and Wilson Reference Barrett and Wilson1981), but this variety is not present in the mid-South rice growing regions (Smith 1970). In California, it is called “late watergrass” because it flowers late in August to September (“late form”) with a close synchrony to rice. This species is an example of a seemingly perfect crop mimic, resembling rice in its morphology and phenology (Vasinger-Alektorova Reference Vasinger-Alektorova1931). Yabuno (Reference Yabuno1966), Gould et al. (Reference Gould, Ali and Fairbrothers1972), Barrett and Seaman (Reference Barrett and Seaman1980), and later followed by Yamasue (Reference Yamasue2001), were not sure of the ploidy status of this variety, and they identified it as a variety of barnyardgrass, although Crampton (Reference Crampton1964) and Yabuno (Reference Yabuno1966) previously differentiated and elevated this taxon to late watergrass.

Strikingly different from barnyardgrass and late watergrass is early watergrass, 2n = 6x = 54 (sometimes previously identified as E. crus-galli var. oryzicola or E. oryzoides). It has defining features such as long awns, and lacks visible anthocyanin pigments. Nevertheless, it was considered a part of the variation encompassed within barnyardgrass prior to the 1980s in California, as implied by Barrett and Wilson (Reference Barrett and Seaman1980). This variety is confined to rice fields in California, with its prominent erect plant architecture and drooping inflorescence. There had been some confusion regarding the taxonomic classification of early watergrass and late watergrass. Barrett and Seaman (Reference Barrett and Seaman1980) wrote that two morphologically and phenologically distinct forms of watergrass exist in California (the “early form” and the “late form”), and considered both forms to be under the same variety despite the fact that Yabuno (Reference Yabuno1984) elucidated, from cytological and morphological studies, that early watergrass is closely related to barnyardgrass, leading to the suggestion that early watergrass be relegated to a variety of barnyardgrass, which was apparently not well received by researchers around the world. However, the recent genome-based global delimitation of Echinochloa species by Wu et al. (Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022) places the “early form” in a separate variety of E. crus-galli (hence, E. crus-galli var. oryzoides), corroborating the classification reported by Yabuno (Reference Yabuno1984), and as opposed to earlier classification as E. oryzoides (Ard.) Fritsch by Vickery (Reference Vickery1975), Chirila and Melachrinos (Reference Chirila and Melachrinos1976), and Clayton (Reference Clayton and Tutin1980).

Although Yabuno (Reference Yabuno1966) suggested that barnyardgrass is an allohexaploid produced by natural hybridization between the tetraploid late watergrass with a not-yet-discovered diploid species of Echinochloa and subsequent chromosome doubling, it was not clear until Ye et al. (Reference Ye, Wu, Mao, Jia, Qiu, Lao, Chen, Jiang, Tang, Peng, Pan, Wang, Feng, Guo and Zhang2020) and Wu et al. (Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022) revealed the evolutionary trajectory of barnyardgrass and other species and varieties of the genus Echinochloa (Figure 1A). Ye et al. (Reference Ye, Wu, Mao, Jia, Qiu, Lao, Chen, Jiang, Tang, Peng, Pan, Wang, Feng, Guo and Zhang2020) found that the diploid genome of E. haploclada (Stapf) Stapf is similar to the unknown diploid progenitor genome of barnyardgrass and used it as a female proxy progenitor. Late watergrass was assumed to be a male donor in the polyploidization of hexaploid barnyardgrass (Akoi and Yamaguchi Reference Aoki and Yamaguchi2008), but recent chloroplast phylogeny analysis indicated that at least two male donors contributed to the origin of barnyardgrass (Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022). The whole-plant and a typical seed and inflorescence morphology of barnyardgrass are shown in Figure 1 B and C, respectively.

Figure 1. Economically most relevant Echinochloa in U.S. rice fields. (A) Origin of barnyardgrass (E. crus-galli var. crus-galli) (adapted from Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022; Ye et al. Reference Ye, Wu, Mao, Jia, Qiu, Lao, Chen, Jiang, Tang, Peng, Pan, Wang, Feng, Guo and Zhang2020). (B) Intrapopulation variation in whole plant morphology of a barnyardgrass population from California (adapted from Norris Reference Norris1996). (C) A typical seed and inflorescence morphology of barnyardgrass (adapted from Jepson Flora Project). Adapted with permission.

Seed Size and Ecological Differentiation

The four Echinochloa species that are of major concern in U.S. rice production, in order of ascending seed size, are junglerice, barnyardgrass, late watergrass, and early watergrass (Costea and Tardif Reference Costea and Tardif2002; Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022; Figure 2A). Seed sizes vary to some extent, with barnyardgrass being the most diverse. Barnyardgrass in California generally produces bigger seeds, as heavy as 3 mg (Keeley and Thullen Reference Keeley and Thullen1989). Junglerice and barnyardgrass seed germination is relatively water intolerant, as explained below, making these weeds common in the predominantly dry-seeded mid-South rice fields (Jones Reference Jones1952). Conversely, early watergrass and late watergrass seed germination is flood tolerant and found in water-seeded California rice (Kennedy et al. Reference Kennedy, Barrett, Vander Zee and Rumpho1980). Seedling emergence generally decreases with increasing depth, and to a greater extent, under flooding conditions (discussed in the Seed Germination and Seedling Emergence section). A generalized scheme of their ecological differentiation is shown in Figure 2B. The consequence of flooding (submergence) is anoxia in plant tissues, which in turn, reduces the rate of energy production by 65% to 97% compared with the rate in air (Gibbs and Greenway Reference Gibbs and Greenway2003). Like rice, early watergrass and late watergrass can germinate under the reduced oxygen of submerged conditions (Kennedy et al. Reference Kennedy, Barrett, Vander Zee and Rumpho1980; Pearce and Jackson Reference Pearce and Jackson1991; VanderZee and Kennedy Reference Kennedy1981) through an array of metabolic adaptations (Kennedy et al. Reference Kennedy, Rumpho and Fox1992).

Figure 2. Seed size in relation to ecological differentiation in Echinochloa species. (A) Caryopsis size of three Echinochloa species (left, adapted from Costea and Tardif Reference Costea and Tardif2002) and seed size distribution of the global collection of Echinochloa species (right, adapted from Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022). (B) Flood as an ecological determinant for the emergence and establishment of Echinochloa species along with the effect of seed placement in the soil profile.

Echinochloa Interference and Seed Production

Interference with Rice

Echinochloa species have co-existed and co-evolved with rice for millennia (Guo et al. Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017), and they have been competitive against both primitive rice and modern, high-yielding rice varieties. Such was probably not the case everywhere; Echinochloa once threatened large-scale commercial rice production in California (Chambliss Reference Chambliss1915; Jones Reference Jones1926). Impacts of barnyardgrass interference have been documented in literature from various parts of the world in several crops (reviewed in Bajwa et al. Reference Bajwa, Jabran, Shahid, Ali and Chauhan2015). In the United States, season-long interference from barnyardgrass can reduce rice yield by up to 70% (Smith 1988). Interference by barnyardgrass at 50 plants m⁻² reduced rice yields of a short-statured cultivar and a semidwarf cultivar by 28% and 65%, respectively, from season-long competition, and barnyardgrass densities of 5 to 10 plants m⁻² were determined to be economic thresholds for short-statured rice cultivars (Stauber et al. Reference Stauber, Smith and Talbert1991). Among semidwarf cultivars, those with a longer maturity period competed more effectively with barnyardgrass (Smith 1974). In a water-seeded culture in California, barnyardgrass at a density of 86 plants m⁻² reduced rice grain yields by 50% (Hill et al. Reference Hill, LeStrange, Bayer and Williams1985). Previously, it was reported that the density of barnyardgrass is more important than the density of rice for the outcome of the competition in terms of rice yield loss and rice panicle number (Smith 1968; Figure 3A). These results were later further supported by Ottis and Talbert (Reference Ottis and Talbert2007) and by Ni et al. (Reference Ni and Robles2004) on relatively advanced rice varieties, indicating no or little scope for using crop density as a management strategy for barnyardgrass. It is noteworthy that barnyardgrass has the potential to cause complete yield loss in rice (Johnson et al. Reference Johnson, Dingkuhn, Jones and Mahamane1998) and nearly total crop failure in cotton (Gossypium hirsutum L.) (Keeley and Thullen Reference Keeley and Thullen1991).

Figure 3. Echinochloa against rice. (A) Competitive outcome of barnyardgrass and rice competition in terms of panicle number and grain yield at varying densities (adapted from Smith 1968). (B) Photosynthetic output of Echinochloa species at increasing CO₂ concentration in comparison with rice (a. barnyardgrass, b. early watergrass, c. late watergrass, and d. rice; adapted from Bouhache and Bayer Reference Bouhache and Bayer1993). (C) Inhibition of rice seedlings by 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) extracted from barnyardgrass seedlings (adapted from Guo et al. Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017).

Late watergrass, a common Echinochloa species in water-seeded California rice, causes up to 50% rice yield losses (Barrett Reference Barrett1983). Interference by one plant of late watergrass with rice in California was 2.3 times greater than intraspecific interference by one rice plant, and the interference was mostly driven by root interactions (Boddy et al. Reference Boddy, Streibig, Yamasue and Fischer2012). In that study, late watergrass plants placed their roots deeper and on average produced seven times more root dry weight than a widely used short-stature modern japonica-type rice cultivar, indicating a remarkable niche differentiation between the two species. When plots were kept free of weeds, including Echinochloa species, for 30 d or longer during a field experiment in California, rice yields were not affected (Gibson et al. Reference Gibson, Fischer, Foin and Hill2002). That finding leads to the suggestion that management strategies that delay the germination or growth of Echinochloa species relative to rice may give the crop a significant competitive advantage. Early competition from barnyardgrass for up to 20 d did not cause any rice yield loss in Arkansas (Smith 1974). The interactions between weed and crop could be influenced by several variables, two of which would be maturity of the crop and crop stature.

According to a recent genomic analysis, Echinochloa lost a considerable portion of disease-resistance genes during polyploidization, indicating that natural selection may prefer a lower investment in the resistance in this weed to maximize its growth and reproduction (Ye et al. Reference Ye, Wu, Mao, Jia, Qiu, Lao, Chen, Jiang, Tang, Peng, Pan, Wang, Feng, Guo and Zhang2020). The next paragraphs highlight the two distinctive characteristics that Echinochloa species possess that allow them to successfully compete with rice.

C₄ Photosynthesis

Echinochloa species possess C₄ photosynthetic cellular machinery. Bouhache and Bayer (Reference Bouhache and Bayer1993) studied photosynthetic characteristics of rice (C₃) and three species of Echinochloa to determine how these characteristics vary with changes in light (Figure 3B) and temperature. Echinochloa species showed higher photosynthetic activity than rice as indicated by both plants’ response to changes in intercellular partial CO₂ pressure, light, and leaf temperature. A C₄-specific carbon fixation enzyme in conjunction with spatially separated photosynthesis phases with Kranz anatomy ensures high photosynthetic efficiency in C₄ plants (Cui Reference Cui2021; Sage et al. Reference Sage, Sage and Kocacinar2012), providing ostensible competitive advantages such as higher rates of CO₂ fixation, decreased photorespiration, and reduced transpiration (Elmore and Paul Reference Elmore and Paul1983). However, the C₄ feature does not confer a universal selective advantage (Elmore and Paul Reference Elmore and Paul1983). Rather, a C₄ weed should have a competitive advantage over crop species under many field situations, such as under high light intensities and temperatures, and in dry conditions (Elmore and Paul Reference Elmore and Paul1983). Black et al. (Reference Black, Chen and Brown1969) also suggested that C₄ photosynthesis may be associated with the more competitive weeds. As is the situation when both weeds and crops are acclimated to the same growth conditions, the C₄ weed frequently overwhelms the crop (Holm et al. Reference Holm, Plucknett, Pancho and Herberger1977) due to its higher net photosynthetic rate, which drives biomass production and reduces environmental stressors in C₄ plants, whereas these stressors are more readily experienced in C₃ species (Elmore and Paul Reference Elmore and Paul1983). Estimates suggest that the photosynthetic efficiency of C₃ plants is less than 4.6%, whereas it can reach over 6% in C₄ plants (Zhu et al., Reference Zhu, Long and Ort2008). Moreover, C₄ plants are known to use water and nitrogen resources more effectively than C₃ plants (Cui Reference Cui2021).

Allelopathy

Recent studies have shed insight on how barnyardgrass interacts with rice. In response to rice allelopathy, barnyardgrass is thought to respond by inhibiting the signal transduction of plant hormones (Fang et al. Reference Fang, Li, Li, Li, Ren, Zheng, Zeng, Shen and Lin2015). Recently, three functional copies of the 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) synthesis gene cluster have been discovered in barnyardgrass (Guo et al. Reference Guo, Qiu, Li, Lu, Olsen and Fan2018). DIMBOA or its analogs are the predominant representatives of benzoxazinoids in plants (Frey et al. Reference Frey, Schullehner, Dick, Fiesselmann and Gierl2009), which function as allelopathic compounds against rice in the field (Guo et al. Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017). When barnyardgrass was cocultured with rice, transcriptomic analysis showed that expression of genes implicated in metabolic pathways and those associated with cytochrome p450 monooxygenases (CYPs) were enriched and elevated (Guo et al. Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017). Also, the allelochemical DIMBOA gene cluster was activated in response to co-cultivation with rice (Guo et al. Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017), indicating a key role for DIMBOA in competitive interactions with rice (Guo et al. Reference Guo, Qiu, Li, Lu, Olsen and Fan2018). As low as a 0.08 mM concentration of DIMBOA inhibited rice height and biomass in laboratory conditions (Guo et al. Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017; Figure 3C). Intriguingly, a gene cluster for momilactone A synthesis in barnyardgrass concurrently expressed more after a fungal pathogen infection, indicating that cohabiting with rice benefits barnyardgrass because of enhanced resistance to blast-infection (Guo et al. Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017, Reference Guo, Qiu, Li, Lu, Olsen and Fan2018).

Seed Dormancy, Germination, and Seedling Emergence

Seed Germination and Seedling Emergence

Seedling emergence is a manifestation of the dormancy status, germination requirements, and growth of seedlings to the surface (Vleeshouwers and Kropff Reference Vleeshouwers and Kropff2000). It is one of the most important demographic events in the life cycle of an annual plant species because the emergence timing determines its survival and reproductive success (Forcella et al. Reference Forcella, Benech-Arnold, Sanchez and Ghersa2000), and this is especially true for agricultural weeds. Much research has occurred since the 1930s to understand the effect of manipulation of moisture and seeding depth on Echinochloa emergence. Important research findings on aspects that have shaped today’s rice production practices and been the major determinant of the population dynamics of Echinochloa species are highlighted below.

Common varieties of Californian barnyardgrass populations seeded on puddled soil emerged to a 100% stand, but those submerged 5, 10, 15, 20, and 25 cm emerged to a 10%, 5%, 1%, 0%, and 0% stand, respectively (Jones Reference Jones1933). Later, in the 1960s, it became apparent that some Echinochloa plants were emerging through the water-flooded rice fields. Barrett and Wilson (Reference Barrett and Wilson1983) studied the effects of soil moisture and seed burial depth on two Echinochloa species, barnyardgrass and late watergrass. When soil moisture was at field capacity, the seeds of both types germinated equally well at all depths, but the maximum number of seedlings emerged from 1- to 2-cm depths. Seedling emergence decreased with the depth below 2 cm, reaching zero at 10-cm depth. The emergence occurred first at shallower depths. Most of the surface-lying seeds that germinated failed to produce seedlings, probably because of a lack of moisture. In saturated soils, however, seed burial caused a reduction in the rate of emergence even at 0.5- to 2-cm depths; seedling emergence was significantly greater at all burial depths in late watergrass as compared to barnyardgrass; and no seedling emergence in barnyardgrass occurred from 2 cm or deeper depths.

In another study, seedling emergence of late watergrass was also greater than barnyardgrass from soil flooded to 9- and 18-cm water depths (Barrett Reference Barrett1983). Anaerobically grown late watergrass seeds are metabolically active, which may explain their ability to emerge from flooded rice fields (Kennedy et al. Reference Kennedy, Barrett, Vander Zee and Rumpho1980). In a pot culture experiment with Crowley silt loam soil in Stuttgart, Arkansas, seedling emergence of barnyardgrass decreased by 90% with flooding to 1.3 cm (Smith and Fox Reference Smith and Fox1973). Arai and Matsunaka (Reference Arai and Matsunaka1966) reported that when the soil moisture content was 70% to 80% of field capacity, a Japanese population of barnyardgrass seed germinated as deep as 10 cm in the soil. But when the soil was submerged, the seeds germinated only in the top 2 cm of soil. The seedling emergence of barnyardgrass was greatest from shallow depths of 1 to 2 cm in a fine, sandy loam soil (Dawson and Bruns Reference Dawson and Bruns1962), and the best germination occurred at 70% to 90% field capacity (Arai and Miyahara Reference Arai and Miyahara1963; Brod Reference Brod1968). The relatively large seeds of Californian barnyardgrass (weighing up to 3 mg) have been reported to emerge (up to 16%) from 10.1 cm or deeper depths under nonflooded conditions (Keeley and Thullen Reference Keeley and Thullen1989). Collectively, these results give insight into how moisture and seeding depth affects emergence of Echinochloa species (Figure 2B).

Several other factors have been shown to affect Echinochloa emergence. Seeds in which dormancy had been broken (1 yr old) germinated best with continued exposure to light (60%) as compared with continuous darkness (6%) (Rahn et al. Reference Rahn, Sweet, Vengris and Dunn1968). More mature (dark gray, brownish, and shiny) seeds produced significantly greater germination than immature (light gray) seeds (Rahn et al. Reference Rahn, Sweet, Vengris and Dunn1968). The seeds may germinate at a wide soil pH range of 4.1 to 8.3 (Arai and Miyahara Reference Arai and Miyahara1963), but the optimal pH for germination is around neutral (Brod Reference Brod1968). Echinochloa species seeded 30 d after rice in a field experiment in California did not survive (Gibson et al. Reference Gibson, Fischer, Foin and Hill2002). No reduction in germination of seeds buried in submerged soil for 30 mo was observed by Roché and Muzik (Reference Roché and Muzik1964); however, seeds buried at 10- and 20-cm depths under nonflooded soil conditions for the same period lost considerable viability. Dawson and Bruns (Reference Dawson and Bruns1975) buried seeds of barnyardgrass at 2.5-, 10-, and 20-cm depths in irrigated and nonirrigated sandy loam soil, and they showed that seeds exhumed from 10- to 20-cm depths had highest germination rates in the second year after burial. The seeds buried for 13 yr had 3% viability but those buried for 15 yr were nonviable. Seeds buried at a 20-cm depth remained viable for a longer period than at 10 cm probably because of greater induced dormancy (Roché and Muzik Reference Roché and Muzik1964). Germination was more rapid in sandy loam rather than loam soil, and soil compacted by tamping and surface watering in a greenhouse produced a higher germination rate (Rahn et al. Reference Rahn, Sweet, Vengris and Dunn1968). Robert et al. (Reference Robert, Vezeau and Simon1983) showed thermal adaptation and acclimation of barnyardgrass at the enzyme level, especially in populations collected from warmer locations. A recent report from Europe indicates that adaptation to local environmental conditions leads to interpopulation differences in base temperature, which affects the emergence process in barnyardgrass (Royo-Esnal et al. Reference Royo-Esnal, Onofri, Taab, Loddo, Necajeva, Uludag, Synowiec, Calha, Lars, Jensen, Uremis, Economou, Murdoch and Tørresen2022). Barnyardgrass seeds were found to germinate in a wide soil pH range of 4.7 to 8.3 (Maun and Barrett Reference Maun and Barrett1986). Laboratory studies on junglerice in the Philippines determined that temperature, light, salt, osmotic stress, soil pH, seed burial depth, and rice residue influenced its germination and emergence (Chauhan and Johnson Reference Chauhan and Johnson2009 ).

In a study on naturally occurring seedbanks in Arkansas, barnyardgrass exhibited an extended period of emergence, with emergence varying widely in the initiation time and the duration across sites and years (Bagavathiannan et al. Reference Bagavathiannan, Norsworthy, Smith and Burgos2011). Such variation was attributed to corresponding rainfall events; however, the vertical distribution of seed in the soil profile was not considered, which is one of the key components to be considered for emergence modeling (Grundy et al. Reference Grundy, Mead and Burston2003). The two contrasting emergence patterns along with relative crop planting time in Arkansas are shown in Figure 4 A and B. Nonetheless, seedling emergence patterns may also be strongly affected by differences in seed dormancy and burial depth and may vary among populations (reviewed in Grundy Reference Grundy2003). Accurate prediction of barnyardgrass emergence, however, will require experiments that adequately control the sources of such variations (Bagavathiannan et al. Reference Bagavathiannan, Norsworthy, Smith and Burgos2011). In California, late watergrass populations emerge in a biphasic pattern, and the ability to model the second phase of the biphasic emergence curve is necessary (Brim-DeForest et al. Reference Brim-DeForest, Al-Khatib and Fischer2022).

Figure 4. Emergence of barnyardgrass in relation to rice/soybean planting time in Arkansas. (A) Rice/soybean planting progress in 2022 (adapted from USDA-NAAS 2022). (B) Barnyardgrass weekly emergence at two sites in Arkansas in 2008 (adapted from Bagavathiannan et al. Reference Bagavathiannan, Norsworthy, Smith and Burgos2011). *Percentage of total seasonal emergence.

Echinochloa – A Persistent Issue in US Rice

Considering that all the economically relevant Echinochloa in U.S. rice production are introduced species and have persisted through the most advanced weed management tools at our disposal, revisiting the historical trajectory of their agroecology is important. Broadly, water management and the use of herbicides that shaped the agroecosystem can be attributed as the determinants driving their population dynamics over the course of the century-long history of U.S. rice production (Figure 5).

Figure 5. Historical trajectory of Echinochloa establishment in U.S. rice crops with milestones in its management. Following multiple introductions, the population dynamics of Echinochloa in U.S. rice have been primarily driven by water management and the use of herbicides. Water-seeding rice culture was developed in the 1920s to reduce infestations of barnyardgrass in rice fields. The widespread use of 2,4-D to control broadleaf weeds in the 1950s favored Echinochloa. Producers in the mid-South shifted to dry-seeding rice after propanil became available in the early 1960s, when barnyardgrass became the keystone rice weed. The long-established water-seeded monoculture of California rice was selected for large-seeded, water-tolerant late watergrass. For the past 50 yr, these species have prevailed in their respective regions with the evolution of resistance to almost all major herbicides that were deployed through the decades, leading to the increased abundance of Echinochloa in U.S. rice. Recent reports indicate an increase in barnyardgrass in California and junglerice in mid-South rice in the last two decades. MHR, multiple herbicide resistance.

In the USDA Farmer’s Bulletin (#688), published within 3 yr of commencement of rice culture in California, CE Chambliss (Reference Chambliss1915) wrote “In three seasons, this weed has become a menace to the rice crop of Sacramento Valley, and unless serious action is taken for its control or eradication its presence may seriously affect the normal development of the rice industry of the state. This may be effectively done through county or community organizations with police power.” In the same bulletin Chambliss mentioned that some farmers spent more than 25% of the total cost of rice production just to manually control the weed. However, according to the reports from the 1930s and 1950s (Jones Reference Jones1938, Reference Jones1952), Echinochloa was not among the top five weeds in the early years of commercial rice cultivation in the mid-South. The water-seeding and continuously flooded rice culture that was developed in 1920s was the savior of the young California rice industry that was threatened by barnyardgrass. This method, in which water is maintained on the fields to a depth of 8 to 20 cm for the duration of rice growth, helped to reduce infestations of barnyardgrass in rice fields (Jones Reference Jones1923, Reference Jones1933).

Because rice grew and yielded well in a water-seeding culture, this method became popular in California in the 1920s (Jones Reference Jones1933) and later spread to the southern rice-growing area to control Echinochloa species (Smith and Fox Reference Smith and Fox1973). Right before the introduction of propanil, the widespread use of 2,4-D to control dicotyledonous weeds in the 1950s favored Echinochloa (Holm et al. Reference Holm, Plucknett, Pancho and Herberger1977) in U.S. rice fields, by creating an opportunity for, and an aggressive population shift to, grassy weeds; like the proliferation of Setaria species in U.S. corn and soybean fields (Oliver and Schreiber Reference Oliver and Schreiber1971; Warwick Reference Warwick1990). California rice remained predominantly water-seeded; however, mid-South rice producers shifted to dry-seeding after propanil became available to control a broad spectrum of weeds.

Since then, it was apparent that Echinochloa species, particularly barnyardgrass, became the keystone species in the mid-South (Smith 1970). A well-developed seed dormancy, as noted earliest by Rahn et al. (Reference Rahn, Sweet, Vengris and Dunn1968) and Holm et al. (Reference Holm, Plucknett, Pancho and Herberger1977), as well as the slower rate of dormancy decay in barnyardgrass, according to Cohen’s prediction (Cohen Reference Cohen1966) are the traits to be selected in habitats where the risk of failure is high from propanil use (Barrett and Wilson Reference Barrett and Wilson1981). In contrast, the relatively rapid decay of dormancy and the synchronous germination in early watergrass and late watergrass are traits that Cohen (Reference Cohen1966) and Harper (Reference Harper1977) both predicted to be selected in a homogeneous environment where the probability of successful reproduction is high (Barrett and Seaman Reference Barrett and Seaman1980). The water-seeded monoculture Californian rice agroecosystem is an excellent example of a homogeneous environment. The predictability of the rice field ecosystem from year to year enabled these water-tolerant species to build up rapidly and favored their spread throughout the rice-growing areas of California, where they persisted in most rice fields despite attempts at control by herbicides (Barrett and Seaman Reference Barrett and Seaman1980). Additionally, the large seeds of late watergrass probably enhanced their competitive ability and favored coexistence with rice; they may have originally been selected as an adaptation that enabled seedlings to grow and emerge in a natural habitat with deep water (Barrett Reference Barrett1983). Since late watergrass can establish successfully in deep water, it replaced barnyardgrass as California’s most economically important weed of rice (Barrett Reference Barrett1983; Barrett and Seaman Reference Barrett and Seaman1980). However, as noted by Smith and Fox (Reference Smith and Fox1973), barnyardgrass persisted in shallow-water areas and field borders thereafter. For the past 50 yr, species of Echinochloa, particularly early watergrass and late watergrass in California and barnyardgrass in the mid-South, have prevailed. With the evolution, spread, and prevalence of resistance to almost all the major herbicides deployed, simultaneously or in sequence, as discussed in the later section, it can be assumed that the abundance of Echinochloa in U.S. rice fields has increased compared to that of the era prior to the 1990s.

Insights From Recent Genomic Studies

Three recent genomic studies have shed light on how Echinochloa have evolved as a weed, made adaptations, and interacted with rice. Pertinent information from these studies to a varying extent has been mentioned throughout this article. Guo et al. (Reference Guo, Qiu, Ye, Jin, Mao, Zhang, Yang, Peng, Wang, Jia, Lin, Li, Fu, Liu and Chen2017) for the first time generated a draft genome of barnyardgrass and provided novel insights into the adaptive molecular mechanisms for its survival and invasiveness in rice fields. The study specifically revealed biosynthetic gene clusters responsible for allelopathic compounds and phytoalexin (DIMBOA and momilactones) in the barnyardgrass genome and decoded evolutionary trajectory of coevolution with rice. Ye et al. (Reference Ye, Wu, Mao, Jia, Qiu, Lao, Chen, Jiang, Tang, Peng, Pan, Wang, Feng, Guo and Zhang2020) improved the genome assembly quality by generating PacBio long reads representing ∼86× coverage of the genome with contig and scaffold N50 sizes of 1.57 Mb and 4.09 Mb, respectively. One of the significant discoveries of the genome research was that Echinochloa may have lowered disease resistance in favor of aggressive growth and development. The other study by Wu et al. (Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022) unprecedently distinguished a global collection of Echinochloa species and varieties (a total of 596 samples) by integrating morphological characteristics with multiple pieces of genomic evidence. As highlighted by Wu et al. (Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022), genomic resources made accessible will accelerate research in Echinochloa evolutionary biology, evolution of resistance to herbicides, interaction between the crop and the weed, and the development of novel weed control strategies. These two studies discovered that this hexaploid genome, yet compact (∼1.4 Gb), contains an incredibly large repertoire of genes for enzymes involved in xenobiotic detoxification, including ABC transporters, CYPs, and glutathione S-transferases (GSTs). These genes in barnyardgrass outnumber those typically found in other grass species. These are the major genetic components that are known to contribute to increased capacity to detoxify herbicides (Yu and Powles Reference Yu and Powles2014); hence, the widespread occurrence of herbicide resistance in barnyardgrass is not surprising.

Of particular interest from the study by Wu et al. (Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022) is that the Echinochloa samples collected from U.S. rice fields were more diverse than Echinochloa from other countries, albeit the U.S. samples were collected from a narrow geographic area. The study did not represent any samples from California. Of the 39 samples from the United States, more than one-third were E. crus-galli var. praticola and none of them were barnyardgrass. Such a large representation of a less-known Echinochloa is likely due to the site of collection being far from rice fields. Of the six samples collected from Arkansas, which appeared to be from the same rice field based on GPS coordinates, all were junglerice. Further research with a wide pool of Echinochloa samples from U.S. rice fields is necessary to address this apparent shortcoming. Genomic proximity, tiller angle, and dominant types of three varieties of E. crus-galli are shown in Figure 6 (adapted from Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022). Although the varieties show little differentiation at the genomic level, their plant architecture is quite different. The seed size of E. crus-galli var. praticola is on the lower side of barnyardgrass and it has a very prostrate morphology (Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022).

Figure 6. Tiller and genomic proximity of three E. crus-galli varieties. (A) Distribution of tiller angle, and (B) genomic proximity as defined by reads mapping rates and genome coverage of reads mapped to a reference genome of a barnyardgrass population from China (both A and B adapted from Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022).

Herbicide Resistance in Echinochloa: An Increasingly Serious Issue

For the past three decades, the U.S. rice industry has been experiencing the predicament of an emerging number of herbicide-resistant Echinochloa species, even for those herbicides that have never been used or are rarely used. Several reports of increased abundance of barnyardgrass populations in response to triazine and thiocarbamate herbicides started to appear in the 1970s and 1980s (reviewed in Maun and Barrett Reference Maun and Barrett1986). That it could evolve resistance to herbicides was realized as early as the 1980s (Maun and Barrett Reference Maun and Barrett1986; Mitich Reference Mitich1990), and since then this fact has been implicated in its remarkable persistence in modern rice cropping systems. Most cases of herbicide resistance in Echinochloa in U.S. rice crops have been documented in the International Herbicide Resistant Weed Database (Heap Reference Heap2023).

The first cases of herbicide resistance in two Echinochloa species, early watergrass and late watergrass, came from water-seeded Californian rice in 2000 (Fischer et al. Reference Fischer, Ateh, Bayer and Hill2000a). For reference, herbicide use history from 1990 through 2018 in California rice crops is shown in Figure 7 (California Department of Pesticide Regulation 2022 ). Despite the fact that molinate was the only major grass herbicide used in California, those populations of late watergrass were reported to have resistance to multiple herbicides from different chemical classes and modes of action (MOAs) including molinate, thiobencarb (thiocarbamates), cyhalofop-butyl, fenoxaprop-ethyl (aryloxyphenoxy propionate), bispyribac-sodium (pyrimidinyl benzoate), penoxsulam (trizolopyrimidine sulfonamide), and clomazone (isoxazolidinone) (Fischer et al. Reference Fischer, Ateh, Bayer and Hill2000a, 2000b; Osuna et al. Reference Osuna, Vidotto, Fischer, Bayer, de Prado and Ferrero2002; Ruiz-Santella et al. Reference Ruiz-Santaella, de Prado, Wagner, Fischer and Gerhards2006; Yasuor et al. Reference Yasuor, TenBrook, Tjeerdema and Fischer2008, Reference Yasuor, Osuna, Ortiz, Saldaín, Eckert and Fischer2009). Besides thiocarbamates, all other herbicides were under development at that time. None of the populations were resistant to the less-used herbicide propanil, although they were found to be less sensitive compared to susceptible populations (Fischer et al. Reference Fischer, Bayer, Carriere, Ateh and Yim2000b; Yasuor et al. Reference Yasuor, Milan, Eckert and Fischer2012). Quite surprisingly, the same populations were later found to be resistant to another herbicide that had also never been used, quinclorac (Yasuor et al. Reference Yasuor, Milan, Eckert and Fischer2012). A single, introduced multiple-resistant biotype (“the founder effect,” as termed by Gressel and Segel Reference Gressel and Segel1990) dispersed throughout California under continued use of molinate and/or thiobencarb (Tsuji et al. Reference Tsuji, Fischer, Yoshino, Roel, Hill and Yamasue2003). Recent results from herbicide resistance testing on grower-submitted samples from California rice fields from 2015 to 2020 indicated the presence of multiple resistance in the vast majority of the Echinochloa samples and the occurrence of multiple resistance up to five MOAs (Becerra-Alvarez et al. Reference Becerra-Alvarez, Estrada, Godar and Al-Khatib2022).

Figure 7. Herbicide use history in California rice fields from 1990 to 2018 (data compiled from the California Department of Pesticide Regulation). (A) First-generation rice herbicides (introduced before 2000), and (B) second-generation rice herbicides (introduced after 2000).

Earlier work suggested that the resistance had primarily endowed by enhanced CYP degradation in late watergrass (Osuna et al. Reference Osuna, Vidotto, Fischer, Bayer, de Prado and Ferrero2002; Yun et al. Reference Yun, Yogo, Miura, Yamasue and Fischer2005; Yasuor et al. Reference Yasuor, Osuna, Ortiz, Saldaín, Eckert and Fischer2009), with some role of GST in conjugating herbicides (Bakkali et al. Reference Bakkali, Ruiz-Santaella, Osuna, Wagner, Fischer and de Prado2007). More recently, Fang (Reference Fang, Yuhua Zhang, Liu, Yan, Li and Dong2019) and Iwakami et al. (Reference Iwakami, Endo, Saika, Okuno, Nakamura, Yokoyama, Watanabe, Toki, Uchino and Inamura2014, Reference Iwakami, Kamidate, Yamaguchi, Ishizaka, Endo, Suda, Nagai, Sunohara, Toki, Uchino, Tominaga and Matsumoto2019) further uncovered the role of two cytochrome P450 enzyme (CYP) genes, CYP81A12 and CYP81A21, in imparting resistance to these herbicides from a wide range of classes. Recent studies on the resistant late watergrass by Dimaano et al. (Reference Dimaano, Tominaga and Iwakami2022) demonstrated that resistance to thiobencarb is independent from these CYP genes. In California rice, flooded conditions in the late watergrass populations induces metabolic adaptations (Boddy et al. Reference Boddy, Streibig, Yamasue and Fischer2012) that might lead to the selection of the CYP genes that enable survival after an application of thiobencarb. Additionally, the herbicide bensulfuron-methyl (sulfonylurea) was widely used for controlling broadleaf and sedges in California rice in the 1980s and 1990s; however, it also partially controlled Echinochloa, indicating a sublethal selection from this herbicide (Fischer et al. Reference Fischer, Bayer, Carriere, Ateh and Yim2000b). Most herbicide resistance mechanism studies in California Echinochloa have been conducted primarily on early watergrass and late watergrass. Hybridization among Echinochloa species has been suggested or experimentally shown, including recent genomic investigations that show some degree of gene flow (Bagavathiannan and Norsworthy Reference Bagavathiannan and Norsworthy2014; Marchesi Reference Marchesi2009; Wu et al. Reference Wu, Shen, Jiang, Feng, Tang, Lao, Jia, Lin, Xie, Weng, Dong, Qian, Lin, Xu and Lu2022; Yabuno Reference Yabuno1981).

Herbicide resistance by Echinochloa species in Arkansas has been well documented via routine screening or surveys; for example, by Riar et al. (Reference Riar, Norsworthy, Steckel, Stephenson, Eubank, Bond and Scott2013b), Norsworthy et al. (Reference Norsworthy, Bond and Scott2013), Rouse et al. (Reference Rouse, Roma-Burgos, Norsworthy, Tseng, Starkey and Scott2018), and Butts et al. (Reference Butts, Kouame, Norsworthy and Barber2022), and the early cases of resistance were reviewed by Talbert and Burgos (Reference Talbert and Burgos2007). Resistance to the extensively used acylanilide herbicide propanil in U.S. rice production (Hoagland et al. Reference Hoagland, Norsworthy, Carey and Talbert2004) was reported in Echinochloa populations from several mid-southern regions in the early 1990s (Baltazer and Smith Reference Baltazar and Smith1994; Carey et al. Reference Carey, Duke, Hoagland and Talbert1995a, Reference Carey, Duke, Hoagland and Talbert1995b). Since its commercialization in the 1960s, propanil had remained the primary herbicide for controlling Echinochloa in mid-southern rice for more than three decades (Carey et al. Reference Carey, Duke, Hoagland and Talbert1995b). Introduced in 1992, quinclorac controlled propanil-resistant barnyardgrass effectively when mixed with propanil (Baltazar and Smith Reference Baltazar and Smith1994; Talbert and Burgos Reference Talbert and Burgos2007); however, several biotypes with multiple resistances to propanil and quinclorac had evolved by the early 2000s (Malik et al. Reference Malik, Burgos and Talbert2010), portending evolution of resistance to the next tool, clomazone (Norsworthy et al. Reference Norsworthy, Scott and Smith2007b), essentially threating the economic viability of rice production in the U.S. mid-South (Malik et al. Reference Malik, Burgos and Talbert2010). Thereafter, clomazone was widely used to control propanil- and quinclorac-resistant barnyardgrass (Norsworthy Reference Norsworthy, Burgos, Scott and Smith2007a), and still today remains the major herbicide in mid-southern rice because resistance to this herbicide is not widespread (Norsworthy et al. Reference Norsworthy, Wilson, Scott and Gbur2014; USDA-NAAS 2022). Following the commercialization of imidazolinone-resistant rice, imazethapyr was another option for controlling barnyardgrass (Norsworthy et al. Reference Norsworthy, Burgos, Scott and Smith2007a). However, the instances of overuse of the herbicide, especially without crop rotation and the use of multiple effective herbicide modes of action, led to selection for the acetolactate synthase–resistant barnyardgrass (Norsworthy et al. Reference Norsworthy, Bond and Scott2013; Riar et al. Reference Riar, Norsworthy, Srivastava, Nandula, Bond and Scott2013a, Reference Riar, Norsworthy, Steckel, Stephenson, Eubank, Bond and Scott2013b) in a short time. Once used in nearly half of the rice fields, imazethapyr use has decreased drastically in recent years (USDA-NAAS 2014, 2022).

Herbicide resistance in Arkansas rice fields has continuously increased in frequency and complexity with additional resistance to aryloxyphenoxy propionate herbicides (cyhalofop-butyl, quizalofop-ethyl) among Echinochloa populations, including junglerice (Rouse et al. Reference Rouse, Roma-Burgos, Norsworthy, Tseng, Starkey and Scott2018, Figure 8). The evolution is apparently a consequence of sequential selection with different major herbicide MOAs, starting with propanil followed by quinclorac and others (Rouse et al. Reference Rouse, Roma-Burgos, Norsworthy, Tseng, Starkey and Scott2018), unlike in California rice where simultaneous resistance to multiple MOAs occurred. Recently, resistance to the newly registered rice herbicide, florpyrauxifen-benzyl, has been reported in barnyardgrass (Hwang et al. Reference Hwang, Norsworthy, González-Torralva, Priess, Barber and Butts2022). The mechanism is nontarget site-based and involves hydrolysis of a methoxy group followed by glucose conjugation (Hwang et al. Reference Hwang, Norsworthy, González-Torralva, Priess, Barber and Butts2022; Takano et al. Reference Takano, Scott, Ouse, Zielinski and Schmitzer2023), and it is believed to have evolved under the selection of an older rice herbicide, penoxsulam (Takano et al. Reference Takano, Scott, Ouse, Zielinski and Schmitzer2023). Earlier, a similar case was reported in a population of barnyardgrass from China that had been under penoxsulam selection for several years (Fang et al. Reference Fang, Yuhua Zhang, Liu, Yan, Li and Dong2019).

Figure 8. Resistance profile of Echinochloa species submitted for resistance testing in Arkansas (2010 to 2016) to four commonly used rice herbicides (adapted from Rouse et al. Reference Rouse, Roma-Burgos, Norsworthy, Tseng, Starkey and Scott2018).

Research Efforts in the Nonchemical Weed Management Space

In a recent survey on weed management concerns in Arkansas rice, effective, nonchemical weed management strategies were rated as only moderately important as current research or an educational effort, even though 78% of the respondents reported high concern with herbicide-resistant weeds (Butts et al. Reference Butts, Kouame, Norsworthy and Barber2022). This finding indicates an inadequate appreciation of the fundamental importance of nonchemical approaches for sustainable weed management and indeed suggests that the views of rice producers on weed control need to change considering the expanding herbicide resistance profile in Echinochloa species. It is a fact that the commercialization of highly effective herbicides has de-escalated the scope, opportunities, and advancement of nonchemical approaches to weed management. Nonetheless, research in the 1970s and 1980s reported successful management of barnyardgrass under certain crop production practices, particularly with the use of tillage and crop rotation (reviewed in Maun and Barrett Reference Maun and Barrett1986). Although the greater need for integrated weed management (IWM) has been realized by some researchers (Hill et al. Reference Hill, Smith and Bayer1994), widespread recognition of herbicide resistance as an inevitable consequence has emerged only in the past two decades, and significant research and extension efforts are being placed on nonchemical methods of weed control as a fundamental element of an IWM strategy. Specifically for rice, the use of harvest weed seed control (HWSC) methods and cover crops in the mid-South and alternate dry and wet seeding in California are being considered as potential IWM components of sustainable management of Echinochloa.

Echinochloa in Furrow-Irrigated Rice

Furrow-irrigated rice has rapidly supplanted a significant acreage of conventional rice in recent years in Arkansas (Hardke et al. Reference Hardke, Sha and Bateman2022) and Missouri, driven by its potential benefits in terms of simplifying crop rotations, decreasing expenses, providing more options in crop management, and conserving water. This system creates more temporal and spatial variability in moisture within the field compared to conventional practices. Furrow irrigation is expected to modulate several key factors in Echinochloa such as emergence, interference with rice and other weeds, response to management interventions, and seedbank renewal. This type of irrigation is generally practiced when crops are planted in rotation, such as with soybean. To better comprehend how this production system influences Echinochloa population dynamics, a relatively longer-term study is required, and the ongoing research efforts should also take junglerice as a potential invader of furrow-irrigated fields into consideration.

Future Directions for Research and its Management

In protecting yield loss from weeds, particularly from Echinochloa species, exciting and depressing moments have both occurred over the course of commercial rice production in the United States. While deep water-seeding saved the growing rice industry in the early 20th century, the discovery of chemicals that selectively killed Echinochloa and other weeds in U.S. rice fields has played a vital role in realizing the monumental gain in rice productivity made possible by improved production practices and the use of advanced genotypes in the last six decades. The U.S. rice industry experienced a “golden period” of weed control in the 1980s when just two herbicides, often only one of which was active against Echinochloa, would keep all the weeds in rice fields at bay. In just six decades of chemical weed management, rice growers today have options for more than a half dozen different MOAs to choose from to target Echinochloa (Barber et al. Reference Barber, Butts, Boyd, Cunningham, Selden, Norsworthy, Burgos and Bertucci2022). However, as indicated by the recent herbicide screening assays, many populations of Echinochloa possess resistance to multiple MOAs of herbicides. The selection of multiple herbicide resistance in Echinochloa species has promoted the development or usage of already available herbicides, but they afford only a partial answer to the weed problem. It might seem intuitive that many herbicides are available or becoming available to target Echinochloa, yet herbicides overlap in their target sites, the mechanism that determines their fate within the plant system, and the way that cellular machinery protects against suffering damage from them. Hence, the selection of mechanisms, especially those that confer the ability to metabolize a broad range of chemical classes, has the potential to render multiple herbicides ineffective. Because the number of herbicide options for Echinochloa control is limited, rice production in the U.S. is becoming more vulnerable to losses from these weeds. The need for an IWM strategy to address Echinochloa issues in US rice is evident. For a more Echinochloa-resistant agroecosystem that dilutes selection from chemical intervention measures, dynamic integration of nonchemical components is important and an apparent future direction. Research efforts into nonchemical practices must gain momentum in the United States as well as globally, especially in light of Echinochloa resistance to herbicides, even those recently introduced. As we enter new endeavors for Echinochloa management, a greater understanding is needed of the adaptive features of the seed biology of such ecologically differentiated Echinochloa types/varieties in varying agroecosystems. Effective management of Echinochloa should rely on knowledge of its population dynamics, including its reproductive potential as affected by chemical and nonchemical intervention efforts. Such knowledge will be useful for manipulating several crop production practices as valuable tools in IWM practices.

Our experience with introduced Echinochloa species clearly indicates that spread and local adaptation are continuous, ongoing processes. Fifty years ago, some water-tolerant Echinochloa species were unknown in U.S. rice fields, and for the last four decades, they have been serious concerns in Californian rice fields. Seemingly, some Echinochloa species have been highly adapted to exploit new opportunities provided by changes in management practices in rice fields. It is to be expected that their response to fundamental selection forces such as changes in crop management practices and the consequential evolution to herbicides will continue to determine the future of the Echinochloa species in U.S. rice fields. The features and adaptations that the surviving Echinochloa plants pick up in this fight will continue to be the immediate issues that U.S. rice producers will face. Therefore, Echinochloa management, as with other weeds, involves the management of selection pressures. The past and present of Echinochloa weeds in U.S. rice crops emphasize the need for understanding its future behavior. From a weed management and overall crop production perspective, the biggest needs for Echinochloa management are the prediction of seed dormancy behavior and seedling emergence pattern, identification, and development; and discovering the most effective use of chemical and nonchemical interventions. Finally, Echinochloa seeds must be prevented from returning to the soil. A modeling study suggests that highly effective herbicide applications and any other efforts that minimize seedbank size are vital for preventing herbicide resistance in barnyardgrass (Bagavathiannan et al. Reference Bagavathiannan, Norsworthy, Smith and Neve2014). As highlighted by Bagavathiannan and Norsworthy (Reference Bagavathiannan and Norsworthy2012), such efforts should take late-season seed production into account. It is also crucial that effective control interventions reflect how they affect weed fecundity (Norsworthy et al. Reference Norsworthy, Korres and Bagavathiannan2018).

Research on the diversity in Echinochloa species driven by management practices in recent decades should continue. Properly construed, the apparent increase in abundance of some species/types acknowledges the need to distinguish and respond to them. Studies on a wider selection of samples is needed so as to elucidate the extent of the diversity in the Echinochloa species, which will lead to the development of prudent management strategies. Using genomics, researchers might study how genetic changes, particularity those that associate with their persistence mechanisms in agroecosystems, have occurred after the multiple introductions of Echinochloa species into U.S. rice and how many resulted from hybridizations among them. A comprehensive genome analysis of Echinochloa that have adapted to U.S. rice fields would probably enable the reconstruction of the evolutionary trajectory of Echinochloa species/varieties, shed light on the developmental origins of diversity in morphological and physiological traits since introduction, and pinpoint the scope and significance of gene flow in the diversification of adaptive mechanisms under various cultural and herbicide interventional regimes.

Obvious historical factors that have determined the persistence and abundance of Echinochloa species, varieties, or ecotypes in U.S. rice crops are the seeding method, water management, land preparation, type and use pattern of herbicides, and their interactions. Those are the ecological or crop production factors that matter most, as they can determine whether, when, and where one or the other Echinochloa species fail or prosper; which production systems are resistant or liable to infestation by a particular species or variety; the impacts that they cause; and the approaches through which they can be managed. Long-term studies comparing the reproductive success of a wide pool of Echinochloa species under varying production systems, taking shifting production practices into account, would provide insight for actions that need to be taken to sustainably manage Echinochloa. Recognizing and implementing ecological and evolutionary principles being the central priority, future research and the efforts should, therefore, lead to its sustainable management through 1) a better understanding of their biology and ecology pertinent to their persistence in the rice agroecosystems of the respective regions; 2) reproductive and genetic mechanisms that drive herbicide resistance evolution, especially that of multiple herbicide resistance; and 3) innovations or new approaches that expand the number of control strategies and effectively disrupt the process of their adaptations, including evolution of resistance to herbicides.

Summary

1. 1. The discovery of chemicals that selectively killed Echinochloa and other weeds in U.S. rice fields has played a vital role in protecting yield from the monumentally improved productivity of rice in the past several decades. Yet Echinochloa species have been a constant concern and immediate issue for U.S. rice production.

2. 2. The spread and regional adaptation of Echinochloa species in U.S. rice fields have been a rapid, continuous, and ongoing process. The trajectory of adaptations that the survivors will pick up in the future rice agroecosystems needs to be curtailed with a greater variety of selective forces.

3. 3. The major adaptation—resistance to multiple MOAs—has promoted the development of new or usage of already available herbicides, affording only a partial answer to the weed problem.

4. 4. As new herbicides are not effectively expanding the diversity of selective forces for Echinochloa control, rice production in the United States is becoming more vulnerable to weed losses. Henceforth, “dynamic” integration of nonchemical components into the weed management to a potential level is evidently important.

5. 5. Echinochloa management should rely on knowledge of its population dynamics, including its reproductive potential as affected by chemical and nonchemical intervention efforts.

6. 6. The changing relative abundance and increasing complexities in forms in Echinochloa species in recent decades indicate an urgent need to reduce the ambiguities regarding its extent.

7. 7. A comprehensive analysis of genomes of Echinochloa species/types that have adapted in U.S. rice fields could shed light on the developmental origins of diversity in morphological and physiological traits and pinpoint the scope and significance of gene glow.

8. 8. The seeding method, water management, land preparation, weed control technology, and their interactions are the major determinants of the persistence and abundance of Echinochloa species in U.S. rice production. Future research should lead to sustainable management of Echinochloa through a better understanding of its adaptation and persistence mechanisms, as well as identifying ways to intensify chemical and nonchemical selective forces.