Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T09:23:21.712Z Has data issue: false hasContentIssue false
  • English
  • Français

Seed mass, dormancy and germinability variation among maternal plants of four Arabian halophytes

Published online by Cambridge University Press:  13 June 2022

Arvind Bhatt ,
David J Gallacher ,
Alfredo Jarma-Orozco  and
Marcelo F. Pompelli Open the ORCID record for Marcelo F. Pompelli [Opens in a new window]
Arvind Bhatt*
Affiliation:
Lushan Botanical Garden, Chinese Academy of Science, Jiujiang, China
David J Gallacher
Affiliation:
Drought Resilience Adoption & Innovation Hub, Charles Darwin University, Casuarina, NT 0810, Australia
Alfredo Jarma-Orozco
Affiliation:
Facultad de Ciencias Agricolas, Universidad de Córdoba, Montería, Córdoba, Colombia
Marcelo F. Pompelli*
Affiliation:
Facultad de Ciencias Agricolas, Universidad de Córdoba, Montería, Córdoba, Colombia
*
*Authors for Correspondence: Marcelo F. Pompelli, E-mail: [email protected]; Arvind Bhatt, E-mail: [email protected]
*Authors for Correspondence: Marcelo F. Pompelli, E-mail: [email protected]; Arvind Bhatt, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Coastal desert vegetation of the Arabian Peninsula is almost entirely dominated by halophytes. Natural populations provide a genetic resource for ecological remediation and may also have direct economic value. High intrapopulation variation of seed traits is presumed to increase population persistence in the unpredictable climatic conditions of this hyper-arid desert. We investigated whether intrapopulation variation of seed mass, dormancy and germinability of four species was attributable to maternal individuals. Arthrocnemum macrostachyum, Halothamnus iraquensis, Haloxylon salicornicum and Seidlitzia rosmarinus are commonly distributed Arabian halophytes with differing seed weight variation. All species exhibited a higher germination when exposed daily to 12 h light, compared to seeds in darkness. A higher germination was correlated with a shorter germination time. For H. iraquensis and S. rosmarinus, a shorter germination time was negatively correlated with germination synchrony. H. salicornicum showed the highest intrapopulation variation of seed traits, followed by A. macrostachyum, S. rosmarinus and H. iraqensis. We found that individuals within populations of all the studied species showed variability in germination but the extent of variation was species-specific. The variation in seed mass and germination among the individuals of the studied species may facilitate a temporal distribution of germination, which may reduce the risk of seed bank exhaustion. The results of this study could assist conservation and management by improving the efficiency of seed collection from wild populations of these species.

Keywords

germination parametersmean germination timeprincipal component analysisrehabilitationseed weightsynchrony
Type
Research Paper
Information
Seed Science Research , Volume 32 , Issue 1 , March 2022 , pp. 53 - 61
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abideen, Z, Ansari, R and Khan, MA (2011) Halophytes: potential source of ligno-cellulosic biomass for ethanol production. Biomass and Bioenergy 35, 1818–1822.CrossRefGoogle Scholar
Adar, M, Najih, Y, Gouskir, M, Chebak, A, Mabrouki, M and Bennouna, A (2020) Three PV plants performance analysis using the principal component analysis method. Energy 207, 118315.CrossRefGoogle Scholar
Ali, A, Iqbal, N, Ali, F and Afzal, B (2012) Alternanthera bettzickiana (Regel) G. Nicholson, a potential halophytic ornamental plant: growth and physiological adaptations. Flora – Morphology, Distribution, Functional Ecology of Plants 207, 318–321.CrossRefGoogle Scholar
Allen, E and Alvarez, S (2020) International rules for seed testing 2020. Zürichstr, Bassersdorf, Switzerland, The International Seed Testing Association.Google Scholar
Amiraslani, F and Dragovich, D (2011) Combating desertification in Iran over the last 50 years: an overview of changing approaches. Journal of Environmental Management 92, 1–13.CrossRefGoogle ScholarPubMed
Ashraf, M and Foolad, MR (2005) Pre-sowing seed treatment: a shotgun approach to improve germination growth and crop yield under saline and none saline conditions. Advances in Agronomy 88, 223–271.CrossRefGoogle Scholar
Ashraf, MA, Awan, AR and Mahmood, K (2012) Rehabilitation of saline ecosystems through cultivation of salt tolerant plants. Pakistan Journal of Botany 44, 69–75.Google Scholar
Baloch, HA, DiTommaso, A and Watson, AK (2001) Intrapopulation variation in Abutilon theophrasti seed mass and its relationship to seed germinability. Seed Science Research 11, 335–343.Google Scholar
Bañuelos, JA, Velázquez-Hernández, I, Guerra-Balcázar, M and Arjona, N (2018) Production, characterization and evaluation of the energetic capability of bioethanol from Salicornia Bigelovii as a renewable energy source. Renewable Energy 123, 125–134.CrossRefGoogle Scholar
Baskin, CC and Baskin, JM (2014) Seeds: ecology, biogeography and evolution of dormancy and germination (2nd edn). London, Academic Press.Google Scholar
Benech-Arnold, RL, Sanchez, RA, Forcella, F, Kruk, B and Ghersa, CM (2000) Environmental control of dormancy in weed seed soil banks. Field and Crop Research 67, 105–122.CrossRefGoogle Scholar
Berner, D (2011) Size correction in biology: how reliable are approaches based on (common) principal component analysis? Oecologia 166, 961–971.CrossRefGoogle ScholarPubMed
Bewley, JD, Bradford, KJ, Hilhorst, HWM and Nonogaki, H (2013) Seeds: physiology of development, germination and dormancy (3rd edn). New York, Springer-Verlag.CrossRefGoogle Scholar
Bhatt, A and Santo, A (2016) Germination and recovery of heteromorphic seeds of Atriplex canescens (Amaranthaceae) under increasing salinity. Plant Ecology 217, 1069–1079.CrossRefGoogle Scholar
Bhatt, A, Pérez-García, F, Carón, MM and Gallacher, D (2016) Germination response of Salsola schweinfurthii (Chenopodiaceae) to salinity and winged perianth removal. Seed Science & Technology 44, 428–434.CrossRefGoogle Scholar
Bhatt, A, Phartyal, SS and Nicholas, A (2017a) Ecological role of distinct fruit-wing perianth color in synchronization of seed germination in Haloxylon salicornicum. Plant Species Biology 32, 121–133.CrossRefGoogle Scholar
Bhatt, A, Phartyal, SS, Phondani, PC and Gallacher, D (2017b) Perianth colour dimorphism is related to germination properties and salinity tolerance in Salsola vermiculata in the Arabian deserts. Nordic Journal of Botany 35, 609–617.CrossRefGoogle Scholar
Bhatt, A, Bhat, NR and Thomas, MT (2019a) Germination behavior of Seidlitzia rosmarinus Boiss., a perennial halophyte of Arabian deserts. Agricultural and Natural Resources 53, 348–354.Google Scholar
Bhatt, A, Bhat, NR, Murru, V and Santo, A (2019b) Eco-physiological studies on desert plants: germination of Halothamnus iraqensis Botsch. seeds under different conditions. Journal of Arid Land 11, 75–85.CrossRefGoogle Scholar
Bhatt, A, Bhat, NR, Lozano-Isla, F, Gallacher, D, Santo, A, Batista-Silva, W, Fernandes, D and Pompelli, MF (2019c) Germination asynchrony is increased by dual seed bank presence in two desert perennial halophytes. Botany 97, 639–649.CrossRefGoogle Scholar
Bhatt, A, Batista-Silva, W, Gallacher, DJ and Pompelli, MF (2020a) Germination of Cenchrus ciliaris, Pennisetum divisum, and Panicum turgidum are seasonally dependent. Botany 98, 10.CrossRefGoogle Scholar
Bhatt, A, Bhat, NR, Al-Nasser, A, Caron, MM and Santo, A (2020b) Inter-population variabilities in seed mass and germination of Panicum turgidum and Pennisetum divisum on the desert of Kuwait. Journal of Arid Land 12, 144–153.CrossRefGoogle Scholar
Bidak, LM, Kamal, SA, Halmy, MWA and Heneidy, SZ (2015) Goods and services provided by native plants in desert ecosystems: examples from the northwestern coastal desert of Egypt. Global Ecology and Conservation 3, 433–447.CrossRefGoogle Scholar
Böer, B (1997) An introduction to the climate of the United Arab Emirates. Journal of Arid Environments 35, 3–16.CrossRefGoogle Scholar
Brändle, M, Stadler, J, Klotz, S and Brand, R (2003) Distributional range size of weedy plant species correlated to germination patterns. Ecology 84, 136–144.CrossRefGoogle Scholar
Bu, H, Du, G, Chen, X, Wang, Y, Xu, X and Liu, K (2009) The evolutionary significance of seed germinability in an alpine meadow on the eastern Qinghai-Tibet Plateau. Arctic, Antarctic, and Alpine Research 41, 97–102.CrossRefGoogle Scholar
Burtt, BL and Lewis, P (1954) On the flora of Kuweit: III. Kew Bulletin 9, 377–410.CrossRefGoogle Scholar
Calone, R, Sanoubar, R, Noli, E and Barbanti, L (2020) Assessing Salicornia europaea tolerance to salinity at seed germination stage. Agriculture 10, 29.CrossRefGoogle Scholar
Castillo, JM, Fernández-Baco, L, Castellanos, EM, Luque, CJ, Figueroa, ME and Davy, AJ (2000) Lower limits of Spartina densiflora and S. maritima in a Mediterranean salt marsh determined by differential ecophysiological tolerances. Journal of Ecology 88, 801–812.CrossRefGoogle Scholar
Chesson, P, Gebauer, RLE, Schwinning, S, Huntly, N, Wiegand, K, Ernest, MSK, Sher, A, Novoplansky, A and Weltzin, JF (2004) Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Ecologia 141, 236–256.Google ScholarPubMed
Corte-Real, N, Oliveira, MS, Jarma-Orozco, A, Fernandes, D, dos Santos, MA, Endres, L, Calsa, T Jr and Pompelli, MF (2020) Comparative analysis of salt-induced changes in the leaves proteome of two contrasting Jatropha curcas genotypes. Brazilian Journal of Development 6, 39845–39872.CrossRefGoogle Scholar
Donohue, K, Dorn, LA, Griffith, C, Schmitt, J, Kim, ES and Aguilera, A (2005) Environmental and genetic influences on the germination of Arabidopsis thaliana in the field. Evolution 59, 740–757.Google ScholarPubMed
Donohue, K, Casas, RRD, Burghardt, L, Kovach, K and Willis, CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution, and Systematics 41, 293–319.CrossRefGoogle Scholar
dos Santos, OO, Mendes, KR, Martins, SVC, Batista-Silva, W, dos Santos, MA, Figueirôa, JM, Souza, ER, Fernandes, D, Araújo, WL and Pompelli, MF (2019) Physiological parameters and plasticity as key factors to understand pioneer and late successional species in the Atlantic Rainforest. Acta Physiologia Plantarum 41, 145.CrossRefGoogle Scholar
El-Keblawy, A and Bhatt, A (2015) Aerial seed bank affects germination in two small-seeded halophytes in Arab Gulf desert. Journal of Arid Environments 117, 10–17.CrossRefGoogle Scholar
El-Keblawy, A, Bhatt, A and Gairola, S (2013) Perianth colour affects germination behavior in the wind pollinated Salsola rubescens in the Arabian Deserts. Botany 92, 69–75.CrossRefGoogle Scholar
El-Keblawy, A, Gairola, S and Bhatt, A (2016a) Maternal habitat affects germination requirements of Anabasis setifera, a succulent shrub of the Arabian deserts. Acta Botanica Brasilica 30, 35–40.CrossRefGoogle Scholar
El-Keblawy, A, Gairola, S and Bhatt, A (2016b) Maternal salinity environment affects salt tolerance during germination in Anabasis setifera: a facultative desert halophyte. Journal of Arid Land 8, 254–263.CrossRefGoogle Scholar
El-Keblawy, A, Gairola, S, Bhatt, A and Mahmoud, T (2017) Effects of maternal salinity on salt tolerance during germination of Suaedaa egyptiaca: a facultative halophyte in the Arab Gulf desert. Plant Species Biology 32, 45–53.CrossRefGoogle Scholar
El-Keblawy, A, Al-Shamsi, N and Mosa, KA (2018) Effect of maternal habitat, temperature and light on germination and salt tolerance of Suaeda vermiculata, a habitat-indifferent halophyte of arid Arabian deserts. Seed Science Research 28, 140–147.CrossRefGoogle Scholar
El Shaer, HM (2010) Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region. Small Ruminant Research 91, 3–12.CrossRefGoogle Scholar
Elnaggar, A, El-Keblawy, A, Mosa, KA and Navarro, T (2019) Adaptive drought tolerance during germination of Salsola drummondii seeds from saline and nonsaline habitats of the arid Arabian deserts. Botany 97, 123–133.CrossRefGoogle Scholar
Freitag, H, Atamov, V, Çetin, E and Aslan, M (2009) The genus Halothamnus Jaub. & Spach (Chenopodiaceae) in Turkey. Turkish Journal of Botany 33, 325–334.Google Scholar
Gairola, S, Bhatt, A and El-Keblawy, A (2015) A perspective on potential use of halophytes for reclamation of salt-affected lands. Wulfenia 22, 88–97.Google Scholar
Galloway, LF (2002) The effect of maternal phenology on offspring characters in the herbaceous plant Campanula americana. Journal of Ecology 90, 851–858.CrossRefGoogle Scholar
Ghazanfar, SA (2006) Saline and alkaline vegetation of NE Africa and the Arabian Peninsula: an overview, pp. 101–108 in Oztürk, M; Waisel, Y; Khan, MA and Görk, G (Eds) Biosaline agriculture and salinity tolerance in plants. Basel, Switzerland, Birkhaeuser Verlag.CrossRefGoogle Scholar
Ghazanfar, SA, Altundag, E, Yaprak, AE, Osborne, J, Tug, GN and Vural, M (2014) Halophytes of Southwest Asia, pp. 105–133 in Khan, MA; Böer, B; Öztürk, M; Al Abdessalaam, TZ; Clüsener-Godt, M and Gul, B (Eds) Sabkha ecosystems: volume IV: cash crop halophyte and biodiversity conservation. Dordrecht, Springer Science Business Media.CrossRefGoogle Scholar
Ghazanfar, SA, Böer, B, Khulaidi, AWA, El-Keblawy, A and Alateeqi, S (2019) Plants of Sabkha ecosystems of the Arabian Peninsula, pp. 55–80 in Gul, B; Böer, B; Khan, MA; Clüsener-Godt, M and Hameed, A (Eds) Sabkha ecosystems. Benji, Nature Switzerland.CrossRefGoogle Scholar
Graifenberg, A, Botrini, L, Giustiniani, L, Filippi, F and Curadi, M (2003) Tomato growing in saline conditions with biodesalinating plants: Salsola soda L., and Portulaca oleracea L. Acta Horticultarae 609, 301–305.CrossRefGoogle Scholar
Gremer, JR and Venable, DL (2014) Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecology Letters 17, 380–387.CrossRefGoogle Scholar
Gutterman, Y (2000) Maternal effects on seeds during development, pp. 59–84 in Fenner, M (Ed) Seeds: the ecology of regeneration in plant communities (2nd edn). Wallingford, England, CABI Publishing.CrossRefGoogle Scholar
Hawke, MA and Maun, MA (1989) Intrapopulation variation in reproduction and seed mass of a beach annual; Cakile edentula var. lacustris. Journal of Coastal Research 5, 103–112.Google Scholar
Huang, Z, Zhang, X, Zheng, G and Gutterman, Y (2003) Influence of light, temperature, salinity and storage on seed germination of Haloxylon ammodendron. Journal of Arid Environments 55, 453–464.CrossRefGoogle Scholar
Levy, SF, Ziv, N and Siegal, ML (2012) Bet hedging in yeast by heterogeneous, age-correlated expression of a stress protectant. PLoS Biology 10, e1001325.CrossRefGoogle ScholarPubMed
Liu, B, Zhao, D, Zhang, P, Liu, F, Jia, M and Liang, J (2020) Seedling evaluation of six walnut rootstock species originated in China based on principal component analysis and cluster analysis. Scientia Horticulturae 265, 109212.CrossRefGoogle Scholar
Lozano-Isla, F, Campos, MLO, Endres, L and Pompelli, MF (2018) Effects of seed storage time and salt stress on the germination of Jatropha curcas L. Industrial Crops and Products 118, 214–224.CrossRefGoogle Scholar
Mahmoodi, T, Khoshhal, J, Mousavi, SH and Pourkhosravani, M (2013) A comparative evaluation of adaptation of Nebkas to stabilize sand dunes of the desert in Sirjan using AHP model. Iran Journal of Environmental and Erosion Research 2, 24–38.Google Scholar
Manousaki, E and Kalogerakis, N (2011) Halophytes present new opportunities in phytoremediation of heavy metals and saline soils. Industrial & Engineering Chemistry Research 50, 656–660.CrossRefGoogle Scholar
Martin, A, Grzeskowiak, V and Puech, S (1995) Germination variability in three species in disturbed Mediterranean environments. Acta Oecologica 16, 479–490.Google Scholar
Milberg, P, Andersson, L and Thompson, K (2000) Large-seeded species are less dependent on light for germination than small-seeded ones. Seed Science Research 10, 99–104.CrossRefGoogle Scholar
Miranda, RQ, Oliveira, MTP, Correia, RM, Almeida-Cortez, JS and Pompelli, MF (2011) Germination of Prosopis juliflora (Sw) DC seeds after scarification treatments. Plant Species Biology 26, 186–192.CrossRefGoogle Scholar
Mitchell, J, Johnston, IG and Bassel, GW (2017) Variability in seeds: biological, ecological, and agricultural implications. Journal of Experimental Botany 68, 809–817.Google ScholarPubMed
Moncaleano-Escandon, J, Silva, BCF, Silva, SRS, Granja, JA, Alves, MCJL and Pompelli, MF (2013) Germination responses of Jatropha curcas L. seeds to storage and aging. Industrial Crops and Products 44, 684–690.CrossRefGoogle Scholar
Narbona, E, Ortiz, PL and Arista, M (2006) Germination variability and the effect of various pre-treatment on germination in the perennial spurge Euphorbia nicaeensis All. Flora 201, 633–641.CrossRefGoogle Scholar
Nimac, A, Lazarević, B, Petek, M, Vidak, M, Šatović, Z and Carović-Stanko, K (2018) Effects of salinity and seed priming on germination of sea fennel (Crithmum maritimum L.). Agriculturae Conspectus Scientificus 83, 181–185.Google Scholar
Nordborg, M and Bergelson, J (1999) The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. American Journal of Botany 86, 470–475.CrossRefGoogle ScholarPubMed
Omar, SAS, Al-Mutawa, Y and Zaman, S (2007) Vegetation of Kuwait. Kuwait, Kuwait Institute for Scientific Research.Google Scholar
Panta, S, Flowers, T, Lane, P, Doyle, R, Haros, G and Shabala, S (2014) Halophyte agriculture: success stories. Environmental and Experimental Botany 107, 71–83.CrossRefGoogle Scholar
Pérez-García, F (2009) Germination characteristics and intrapopulation variation in carob (Ceratonia siliqua L) seeds. Spanish Journal of Agricultural Research 7, 398–406.CrossRefGoogle Scholar
Phondani, PC, Bhatt, A, Elsarrag, E and Horr, YA (2016) Ethnobotanical magnitude towards sustainable utilization of wild foliage in Arabian Desert. Journal of Traditional and Complementary Medicine 6, 209–218.CrossRefGoogle ScholarPubMed
Platenkamp, GAJ and Shaw, RG (1993) Environmental and genetic maternal effects on seed characters in Nemophila menziesii. Evolution 47, 540–555.CrossRefGoogle ScholarPubMed
Pompelli, MF, Ferreira, DTRG, Cavalcante, PPGS, Salvador, TL, Hsie, BS and Endres, L (2010) Environmental influence on the physico-chemical and physiological properties of Jatropha curcas L. seeds. Australian Journal of Botany 58, 421–427.CrossRefGoogle Scholar
Pompelli, MF, Mendes, KR, Ramos, MV, Santos, JNB, Youssef, DTA, Pereira, JD, Endres, L, Jarma-Orozco, A, Solano-Gomes, R, Jarma-Arroyo, B, Silva, ALJ, Santos, MA and Antunes, WC (2019) Mesophyll thickness and sclerophylly among Calotropis procera morphotypes reveal water-saved adaptation to environments. Journal of Arid Lands 11, 795–810.CrossRefGoogle Scholar
Prabu, R, Vanniarajan, C, Vetrivanthan, M, Gnanamalar, RP, Shanmughasundaram, R and Ramalingam, J (2020) Diversity study using principal component analysis in barnyard millet (Echinochloa frumentacea (Roxb.) Link). Electronic Journal of Plant Breeding 11, 606–609.Google Scholar
Qasim, M, Gulzar, S, Shinwari, ZK, Aziz, I and Khan, MA (2010) Traditional ethnobotanical uses of halophytes from Hub, Balochistan. Pakistan Journal of Botany 42, 1543–1551.Google Scholar
Rabhi, M, Ferchichi, S, Jouini, J, Hamrouni, MH, Koyro, HW, Ranieri, A, Abdelly, C and Smaoui, A (2010) Phytodesalination of a salt-affected soil with the halophyte Sesuvium portulacastrum L. to arrange in advance the requirements for the successful growth of a glycophytic crop. Bioresource Technology 101, 6822–6828.CrossRefGoogle ScholarPubMed
Redondo-Gómez, S, Mateos-Naranjo, E and Andrades-Moreno, L (2010) Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum macrostachyum. Journal of Hazardous Materials 184, 299–307.CrossRefGoogle Scholar
Rojas-Aréchiga, M, Mandujano, MC and Golubov, J (2013) Seed size and photoblastism in species belonging to tribe Cacteae (Cactaceae). Journal of Plant Research 126, 376–386.CrossRefGoogle Scholar
Saatkamp, A, Cochrane, A, Commander, L, Guja, LK, Jimenez-Alfaro, B, Larson, J, Nicotra, A, Poschlod, P, Silveira, FAO, Cross, AT, Dalziell, EL, Dickie, J, Erickson, TE, Fidelis, A, Fuchs, A, Golos, PJ, Hope, M, Lewandrowski, W, Merritt, DJ, Miller, BP, Miller, RG, Offord, CA, Ooi, MKJ, Satyanti, A, Sommerville, KD, Tangney, R, Tomlinson, S, Turner, S and Walck, JL (2019) A research agenda for seed-trait functional ecology. New Phytology 221, 1764–1775.CrossRefGoogle ScholarPubMed
Santelices, R, Espinoza, S, Magni, C, Cabrera, A, Donoso, S and Peña, K (2017) Variability in seed germination and seedling growth at the intra- and inter-provenance levels of Nothofagus glauca (Lophozonia glauca), an endemic species of Central Chile. New Zealand Journal of Forestry Science 47, 10.CrossRefGoogle Scholar
Santo, A, Mattana, E, Grillo, O, Sciandrello, S, Peccenini, S and Bacchetta, G (2017) Variability on morphological and ecological seed traits of Limonium avei (De Not.) Brullo & Erben (Plumbaginaceae). Plant Species Biology 32, 368–337.CrossRefGoogle Scholar
Schütz, W and Milberg, P (1997) Seed dormancy in Carex canescens: regional differences and ecological consequences. Oikos 78, 420–428.CrossRefGoogle Scholar
Slatkin, M (1974) Competition and regional coexistence. Ecology 55, 128–134.CrossRefGoogle Scholar
Song, R, Kelman, D, Johns, KL and Wright, AD (2012) Correlation between leaf age, shade levels, and characteristics beneficial natural constituents of tea (Camelia sinensis) grown in Hawaii. Food Chemistry 133, 707–714.CrossRefGoogle Scholar
Tautenhahn, S, Heilmeier, H, Götzenberger, L, Klotz, S, Wirth, C and Kühn, I (2008) On the biogeography of seed mass in Germany-distribution patterns and environmental correlates. Ecography 31, 457–468.CrossRefGoogle Scholar
Tester, M and Davenport, R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.CrossRefGoogle ScholarPubMed
Tielbörger, K, Petruủ, M and Lampei, C (2012) Bet-hedging germination in annual plants: a sound empirical test of the theoretical foundations. Oikos 121, 1860–1868.CrossRefGoogle Scholar
Torres-Martinez, L, Weldy, P, Levy, M and Emery, NC (2016) Spatiotemporal heterogeneity in precipitation patterns explain population-level germination strategies in an edaphic specialist. Annals of Botany 119, 253–265.CrossRefGoogle Scholar
Wang, L, Wu, Y, Tian, Y, Dai, T, Xie, G, Xu, Y and Chen, F (2020) Overexpressing Jatropha curcas CBF2 in Nicotiana benthamiana improved plant tolerance to drought stress. Gene 742, 144588.CrossRefGoogle ScholarPubMed
Zaidi, CHA, González-Benito, ME and Pérez-García, F (2010) Morphological and physiological seed heterogeneity in the Mediterranean annual plant Tuberaria macrosepala (Cistaceae). Plant Species Biology 25, 149–157.CrossRefGoogle Scholar
Zhao, NX, Zhang, LH, Zhao, TT, Mo, LD, Zhang, JL, Gao, YB and Wang, JL (2016) Trait differentiation among Stipa krylovii populations in the Inner Mongolia Steppe region. Flora 223, 90–98.CrossRefGoogle Scholar
Zia, S and Khan, MA (2004) Effect of light, salinity, and temperature on seed germination of Limonium stocksii. Canadian Journal of Botany 82, 151–157.CrossRefGoogle Scholar