Dormancy and heteromorphism are innate seed properties that control germination timing through adaptation to the prevailing environment. The degree of variation in dormancy depth within a seed population differs considerably depending on the genotype and maternal environment. Dormancy is therefore a key trait of annual weeds to time seedling emergence across seasons. Seed heteromorphism, the production of distinct seed morphs (in color, mass or other morphological characteristics) on the same individual plant, is considered to be a bet-hedging strategy in unpredictable environments. Heteromorphic species evolved independently in several plant families and the distinct seed morphs provide an additional degree of variation. Here we conducted a comparative morphological and molecular analysis of the dimorphic seeds (black and brown) of the Amaranthaceae weed Chenopodium album. Freshly harvested black and brown seeds differed in their dormancy and germination responses to ambient temperature. The black seed morph of seedlot #1 was dormant and 2/3rd of the seed population had non-deep physiological dormancy which was released by after-ripening (AR) or gibberellin (GA) treatment. The deeper dormancy of the remaining 1/3rd non-germinating seeds required in addition ethylene and nitrate for its release. The black seeds of seedlot #2 and the brown seed morphs of both seedlots were non-dormant with 2/3rd of the seeds germinating in the fresh mature state. The dimorphic seeds and seedlots differed in testa (outer seed coat) thickness in that thick testas of black seeds of seedlot #1 conferred coat-imposed dormancy. The dimorphic seeds and seedlots differed in their abscisic acid (ABA) and GA contents in the dry state and during imbibition in that GA biosynthesis was highest in brown seeds and ABA degradation was faster in seedlot #2. Chenopodium genes for GA and ABA metabolism were identified and their distinct transcript expression patterns were quantified in dry and imbibed C. album seeds. Phylogenetic analyses of the Amaranthaceae sequences revealed a high proportion of expanded gene families within the Chenopodium genus. The identified hormonal, molecular and morphological mechanisms and dormancy variation of the dimorphic seeds of C. album and other Amaranthaceae are compared and discussed as adaptations to variable and stressful environments.

Crop Protection Research Syngenta Jealott's Hill International Research Centre Bracknell United Kingdom

Department of Biological Sciences Royal Holloway University of London Egham United Kingdom

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany Czech Academy of Sciences Olomouc Czechia

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Altenhofen L. M., Dekker J. (2013). Complex regulation of Chenopodium album seed germination. Appl. Ecol. Environ. Sci. 1, 133–142. doi: 10.12691/aees-1-6-6 DOI

Arshad W., Lenser T., Wilhelmsson P. K. I., Chandler J. O., Steinbrecher T., Marone F., et al. . (2021). A tale of two morphs: developmental patterns and mechanisms of seed coat differentiation in the dimorphic diaspore model Aethionema arabicum (Brassicaceae). Plant J. 107, 166–181. doi: 10.1111/tpj.15283 PubMed DOI

Bajwa A. A., Zulfiqar U., Sadia S., Bhowmik P., Chauhan B. S. (2019). A global perspective on the biology, impact and management of Chenopodium album and Chenopodium murale: Two troublesome agricultural and environmental weeds. Environ. Sci. pollut. Res. 26, 5357–5371. doi: 10.1007/s11356-018-04104-y PubMed DOI

Baskin C. C., Baskin J. M. (2006). The natural history of soil seed banks of arable land. Weed Sci. 54, 549–557. doi: 10.1614/WS-05-034R.1 DOI

Baskin C. C., Baskin J. M. (2019). Martin's peripheral embryo - unique but not a phylogenetic 'orphan' at the base of his family tree: a tribute to the insight of a pioneer seed biologist. Seed Sci. Res. 29, 155–166. doi: 10.1017/S0960258519000175 DOI

Baskin J. M., Lu J. J., Baskin C. C., Tan D. Y., Wang L. (2014). Diaspore dispersal ability and degree of dormancy in heteromorphic species of cold deserts of northwest China: A review. Perspect. Plant Ecology Evol. Systematics 16, 93–99. doi: 10.1016/j.ppees.2014.02.004 DOI

Batlla D., Benech-Arnold R. L. (2015). A framework for the interpretation of temperature effects on dormancy and germination in seed populations showing dormancy. Seed Sci. Res. 25, 147–158. doi: 10.1017/S0960258514000452 DOI

Batlla D., Ghersa C. M., Benech-Arnold R. L. (2020). Dormancy, a critical trait for weed success in crop production systems. Pest Manage. Sci. 76, 1189–1194. doi: 10.1002/ps.5707 PubMed DOI

Bhatt A., Santo A. (2016). Germination and recovery of heteromorphic seeds of Atriplex canescens (Amaranthaceae) under increasing salinity. Plant Ecol. 217, 1069–1079. doi: 10.1007/s11258-016-0633-6 DOI

Bouwmeester H. J., Karssen C. M. (1989). Environmental factors influencing the expression of dormancy patterns in weed seeds. Ann. Bot. 63, 113–120. doi: 10.1093/oxfordjournals.aob.a087713 DOI

Bouwmeester H. J., Karssen C. M. (1993). Seasonal periodicity in germination of seeds of Chenopodium album l. Ann. Bot. 72, 463–473. doi: 10.1006/anbo.1993.1133 DOI

Bradford K. J. (2002). Applications of hydrothermal time to quantifying and modeling seed germination and dormancy. Weed Sci. 50, 248–260. doi: 10.1614/0043-1745(2002)050[0248:AOHTTQ]2.0.CO;2 DOI

Ceccato D., Bertero D., Batlla D., Galati B. (2015). Structural aspects of dormancy in quinoa (Chenopodium quinoa): importance and possible action mechanisms of the seed coat. Seed Sci. Res. 25, 267–275. doi: 10.1017/S096025851500015X DOI

Chahtane H., Kim W., Lopez-Molina L. (2017). Primary seed dormancy: a temporally multilayered riddle waiting to be unlocked. J. Exp. Bot. 68, 857–869. doi: 10.1093/jxb/erw377 PubMed DOI

Fernández Farnocchia R. B., Benech-Arnold R. L., Mantese A., Battla D. (2021). Optimization of next-generation emergence timing of Amaranthus hybridus is determined through seed dormancy modulation by the maternal environment. J. Exp. Bot. 72, 4283–4297. doi: 10.1093/jxb/erab141 PubMed DOI

Finch-Savage W. E., Leubner-Metzger G. (2006). Seed dormancy and the control of germination. New Phytol. 171, 501–523. doi: 10.1111/j.1469-8137.2006.01787.x PubMed DOI

Finch-Savage W. E., Cadman C. S. C., Toorop P. E., Lynn J. R., Hilhorst H. W. M. (2007). Seed dormancy release in arabidopsis cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J. 51, 60–78. doi: 10.1111/j.1365-313X.2007.03118.x PubMed DOI

Finch-Savage W. E., Footitt S. (2017). Seed dormancy cycling and the regulation of dormancy mechanisms to time germination in variable field environments. J. Exp. Bot. 68, 843–856. doi: 10.1093/jxb/erw477 PubMed DOI

Gardarin A., Dürr C., Mannino M. R., Busset H., Colbach N. (2010). Seed mortality in the soil is related to seed coat thickness. Seed Sci. Res. 20, 243–256. doi: 10.1017/S0960258510000255 DOI

Giacomelli L., Rota-Stabelli O., Masuero D., Acheampong A. K., Moretto M., Caputi L., et al. . (2013). Gibberellin metabolism in Vitis vinifera l. during bloom and fruit-set: functional characterization and evolution of grapevine gibberellin oxidases. J. Exp. Bot. 64, 4403–4419. doi: 10.1093/jxb/ert251 PubMed DOI PMC

Gianella M., Bradford K. J., Guzzon F. (2021). Ecological, (epi)genetic and physiological aspects of bet-hedging in angiosperms. Plant Reprod. 34, 21–36. doi: 10.1007/s00497-020-00402-z PubMed DOI PMC

Goodstein D. M., Shu S. Q., Howson R., Neupane R., Hayes R. D., Fazo J., et al. . (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–D1186. doi: 10.1093/nar/gkr944 PubMed DOI PMC

Graeber K., Linkies A., Wood A. T., Leubner-Metzger G. (2011). A guideline to family-wide comparative state-of-the-art quantitative RT-PCR analysis exemplified with a brassicaceae cross-species seed germination case study. Plant Cell 23, 2045–2063. doi: 10.1105/tpc.111.084103 PubMed DOI PMC

Guillemin J. P., Gardarin A., Granger S., Reibel C., Munier-Jolain N., Colbach N. (2013). Assessing potential germination period of weeds with base temperatures and base water potentials. Weed Res. 53, 76–87. doi: 10.1111/wre.12000 DOI

Hao Y. Q., Hong Y. C., Guo H. M., Qin P. Y., Huang A. N., Yang X. S., et al. . (2022). Transcriptomic and metabolomic landscape of quinoa during seed germination. BMC Plant Biol. 22, 237. doi: 10.1186/s12870-022-03621-w PubMed DOI PMC

Hedden P. (2020). The current status of research on gibberellin biosynthesis. Plant Cell Physiol. 61, 1832–1849. doi: 10.1093/pcp/pcaa092 PubMed DOI PMC

Hermann K., Meinhard J., Dobrev P., Linkies A., Pesek B., Heß B., et al. . (2007). 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris l.) - a comparative study of fruits and seeds. J. Exp. Bot. 58, 3047–3060. doi: 10.1093/jxb/erm162 PubMed DOI

Holloway T., Steinbrecher T., Pérez M., Seville A., Stock D., Nakabayashi K., et al. . (2021). Coleorhiza-enforced seed dormancy: A novel mechanism to control germination in grasses. New Phytol. 229, 2179–2191. doi: 10.1111/nph.16948 PubMed DOI

Hourston J. E., Steinbrecher T., Chandler J. O., Pérez M., Dietrich K., Turečková V., et al. . (2022). Cold-induced secondary dormancy and its regulatory mechanisms in beta vulgaris. Plant Cell Environ. 45, 1315–1332. doi: 10.1111/pce.14264 PubMed DOI PMC

Huang Y., Wang X., Ge S., Rao G. Y. (2015). Divergence and adaptive evolution of the gibberellin oxidase genes in plants. BMC Evolutionary Biol. 15, 207. doi: 10.1186/s12862-015-0490-2 PubMed DOI PMC

Imbert E. (2002). Ecological consequences and ontogeny of seed heteromorphism. Perspect. Plant Ecology Evol. Systematics 5, 13–36. doi: 10.1078/1433-8319-00021 DOI

Jarvis D. E., Ho Y. S., Lightfoot D. J., Schmockel S. M., Li B., Borm T. J. A., et al. . (2017). The genome of Chenopodium quinoa . Nature 542, 307–315. doi: 10.1038/nature21370 PubMed DOI

Kadereit G., Newton R. J., Vandelook F. (2017). Evolutionary ecology of fast seed germination-a case study in Amaranthaceae/Chenopodiaceae. Perspect. Plant Ecol. Evol. Systematics 29, 1–11. doi: 10.1016/j.ppees.2017.09.007 DOI

Karssen C. M. (1968). The light promoted germination of the seeds of Chenopodium album L. - II. Effects of (RS)-abscisic acid. Acta Botanica Neerlandica 17, 293–308. doi: 10.1111/J.1438-8677.1968.TB00129.X DOI

Karssen C. M. (1970). Light promoted germination of seeds of Chenopodium album L . - III. Effect of photoperiod during growth and development of plants on dormancy of produced seeds. Acta Botanica Neerlandica 19, 81–94.

Karssen C. M. (1976. a). Two sites of hormonal action during germination of Chenopodium album seeds. Physiologia Plantarum 36, 264–270. doi: 10.1111/j.1399-3054.1976.tb04426.x DOI

Karssen C. M. (1976. b). Uptake and effect of abscisic acid during induction and progress of radicle growth in seeds of Chenopodium album . Physiologia Plantarum 36, 259–263. doi: 10.1111/j.1399-3054.1976.tb04425.x DOI

Krak K., Habibi F., Douda J., Vit P., Lomonosova M. N., Wang L., et al. . (2019). Human-mediated dispersal of weed species during the Holocene: A case study of Chenopodium album agg. J. Biogeography 46, 1007–1019. doi: 10.1111/jbi.13545 DOI

Krak K., Vit P., Belyayev A., Douda J., Hreusova L., Mandak B. (2016). Allopolyploid origin of Chenopodium album s. str. (Chenopodiaceae): a molecular and cytogenetic insight. PLoS One 11, e0161063. doi: 10.1371/journal.pone.0161063 PubMed DOI PMC

Kushiro T., Okamoto M., Nakabayashi K., Yamagishi K., Kitamura S., Asami T., et al. . (2004). The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'-hydroxylases: key enzymes in ABA catabolism. Eur. Mol. Biol. Organ. J. 23, 1647–1656. doi: 10.1038/sj.emboj.7600121 PubMed DOI PMC

Lange T., Lange M. J. P. (2020). The multifunctional dioxygenases of gibberellin synthesis. Plant Cell Physiol. 61, 1869–1879. doi: 10.1093/pcp/pcaa051 PubMed DOI

Lefebvre V., North H., Frey A., Sotta B., Seo M., Okamoto M., et al. . (2006). Functional analysis of arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J. 45, 309–319. doi: 10.1111/j.1365-313X.2005.02622.x PubMed DOI

Lenser T., Graeber K., Cevik O. S., Adiguzel N., Donmez A. A., Grosche C., et al. . (2016). Developmental control and plasticity of fruit and seed dimorphism in Aethionema arabicum . Plant Physiol. 172, 1691–1707. doi: 10.1104/pp.16.00838 PubMed DOI PMC

Li W., Yamaguchi S., Khan M. A., An P., Liu X., Tran L. S. (2016). Roles of gibberellins and abscisic acid in regulating germination of Suaeda salsa dimorphic seeds under salt stress. Front. Plant Sci. 6, 1235. doi: 10.3389/fpls.2015.01235 PubMed DOI PMC

Li Q. H., Yu X. T., Chen L., Zhao G., Li S. Z., Zhou H., et al. . (2021). Genome-wide identification and expression analysis of the NCED family in cotton (Gossypium hirsutum l.). PLoS One 16, e0246021. doi: 10.1371/journal.pone.0246021 PubMed DOI PMC

Liu R. R., Wang L., Tanveer M., Song J. (2018). Seed heteromorphism: an important adaptation of halophytes for habitat heterogeneity. Front. Plant Sci. 9, 1515. doi: 10.3389/fpls.2018.01515 PubMed DOI PMC

Ma X., Vaistij F. E., Li Y., Van Rensburg W. S. J., Harvey S., Bairu M. W., et al. . (2021). A chromosome-level Amaranthus cruentus genome assembly highlights gene family evolution and biosynthetic gene clusters that may underpin the nutritional value of this traditional crop. Plant J. 107, 613–628. doi: 10.1111/tpj.15298 PubMed DOI

MacGregor D. R., Kendall S. L., Florance H., Fedi F., Moore K., Paszkiewicz K., et al. . (2015). Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism. New Phytol. 205, 642–652. doi: 10.1111/nph.13090 PubMed DOI

Machabée S., Saini H. S. (1991). Differences in the requirement for endogenous ethylene during germination of dormant and non-dormant seeds of Chenopodium album l. J. Plant Physiol. 138, 97–101. doi: 10.1016/S0176-1617(11)80737-6 DOI

Mandak B., Krak K., Vit P., Lomonosova M. N., Belyayev A., Habibi F., et al. . (2018). Hybridization and polyploidization within the Chenopodium album aggregate analysed by means of cytological and molecular markers. Mol. Phylogenet. Evol. 129, 189–201. doi: 10.1016/j.ympev.2018.08.016 PubMed DOI

Matilla A., Gallardo M., Puga-Hermida M. I. (2005). Structural, physiological and molecular aspects of heterogeneity in seeds: a review. Seed Sci. Res. 15, 63–76. doi: 10.1079/SSR2005203 DOI

Matsushima R. (2014). Thin sections of technovit 7100 resin of rice endosperm and staining. Bio-protocol J. 4, e1239. doi: 10.21769/BioProtoc.1239 DOI

Murdoch A. J., Roberts E. H. (1997). Temperature and the rate of germination of dormant seeds of Chenopodium album . Basic Appl. Aspects Seed Biol. 30, 547–553. doi: 10.1007/978-94-011-5716-2_60 DOI

Murdoch A. J., Roberts E. H., Goedert C. O. (1989). A model for germination responses to alternating temperatures. Ann. Bot. 63, 97–111. doi: 10.1093/oxfordjournals.aob.a087733 DOI

Nakabayashi K., Leubner-Metzger G. (2021). Seed dormancy and weed emergence: from simulating environmental change to understanding trait plasticity, adaptive evolution, and population fitness. J. Exp. Bot. 72, 4181–4185. doi: 10.1093/jxb/erab150 PubMed DOI PMC

Nambara E., Okamoto M., Tatematsu K., Yano R., Seo M., Kamiya Y. (2010). Abscisic acid and the control of seed dormany and germination. Seed Sci. Res. 20, 55–67. doi: 10.1017/S0960258510000012 DOI

Neve P., Vila-Aiub M., Roux F. (2009). Evolutionary-thinking in agricultural weed management. New Phytol. 184, 783–793. doi: 10.1111/j.1469-8137.2009.03034.x PubMed DOI

Ogawa M., Hanada A., Yamauchi Y., Kuwahara A., Kamiya Y., Yamaguchi S. (2003). Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15, 1591–1604. doi: 10.1105/tpc.011650 PubMed DOI PMC

Okamoto M., Kuwahara A., Seo M., Kushiro T., Asami T., Hirai N., et al. . (2006). CYP707A1 and CYP707A2, which encode ABA 8'-hydroxylases, are indispensable for a proper control of seed dormancy and germination in arabidopsis. Plant Physiol. 141, 97–107. doi: 10.1104/pp.106.079475 PubMed DOI PMC

Penfield S., MacGregor D. R. (2017). Effects of environmental variation during seed production on seed dormancy and germination. J. Exp. Bot. 68, 819–825. doi: 10.1093/jxb/erw436 PubMed DOI

Prego I., Maldonado S., Otegui M. (1998). Seed structure and localization of reserves in Chenopodium quinoa . Ann. Bot. 82, 481–488. doi: 10.1006/anbo.1998.0704 DOI

Roman E. S., Thomas A. G., Murphy S. D., Swanton C. J. (1999). Modeling germination and seedling elongation of common lambsquarters (Chenopodium album). Weed Sci. 47, 149–155. doi: 10.1017/S0043174500091554 DOI

Sabir I. A., Manzoor M. A., Shah I. H., Abbas F., Liu X. J., Fiaz S., et al. . (2022). Evolutionary and integrative analysis of gibberellin-dioxygenase gene family and their expression profile in three rosaceae genomes (F. vesca, P. mume, and P. avium) under phytohormone stress. Front. Plant Sci. 13, 942969. doi: 10.3389/fpls.2022.942969 PubMed DOI PMC

Saini H. S., Bassi P. K., Spencer M. S. (1985). Seed germination in Chenopodium album l. - relationships between nitrate and the effects of plant hormones. Plant Physiol. 77, 940–943. doi: 10.1104/pp.77.4.940 PubMed DOI PMC

Saitou N., Nei M. (1987). The neighbor-joining method - a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425. doi: 10.1093/oxfordjournals.molbev.a040454 PubMed DOI

Song J., Shi W. W., Liu R. R., Xu Y. G., Sui N., Zhou J. C., et al. . (2017). The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Species Biol. 32, 107–114. doi: 10.1111/1442-1984.12132 DOI

Soureshjani H. K., Bahador M., Tadayon M. R., Dehkordi A. G. (2022). Modeling seed germination of quinoa (Chenopodium quinoa willd.) at different temperatures and water potentials. Acta Physiologiae Plantarum 44, 102. doi: 10.1007/s11738-022-03425-3 DOI

Steckel L. E., Sprague C. L., Stoller E. W., Wax L. M. (2004). Temperature effects on germination of nine amaranthus species. Weed Sci. 52, 217–221. doi: 10.1614/WS-03-012R DOI

Steinbrecher T., Leubner-Metzger G. (2017). The biomechanics of seed germination. J. Exp. Bot. 68, 765–783. doi: 10.1093/jxb/erw428 PubMed DOI

Sukhorukov A. P., Mavrodiev E. V., Struwig M., Nilova M. V., Dzhalilova K. K., Balandin S. A., et al. . (2015). One-seeded fruits in the core caryophyllales: Their origin and structural diversity. PLoS One 10, e0117974. doi: 10.1371/journal.pone.0117974 PubMed DOI PMC

Turečková V., Novák O., Strnad M. (2009). Profiling ABA metabolites in Nicotiana tabacum l. leaves by ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Talanta 80, 390–399. doi: 10.1016/j.talanta.2009.06.027 PubMed DOI

Urbanova T., Tarkowská D., Novák O., Hedden P., Strnad M. (2013). Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112, 85–94. doi: 10.1016/j.talanta.2013.03.068 PubMed DOI

Urbanova T., Tarkowska D., Strnad M., Hedden P. (2011). Gibberellins - terpenoid plant hormones: biological importance and chemical analysis. Collection Czechoslovak Chem. Commun. 76, 1669–1686. doi: 10.1135/cccc2011098 DOI

Vandelook F., Newton R. J., Bobon N., Bohley K., Kadereit G. (2021). Evolution and ecology of seed internal morphology in relation to germination characteristics in amaranthaceae. Ann. Bot. 127, 799–811. doi: 10.1093/aob/mcab012 PubMed DOI PMC

Walck J. L., Hidayati S. N., Dixon K. W., Thompson K., Poschlod P. (2011). Climate change and plant regeneration from seed. Global Change Biol. 17, 2145–2161. doi: 10.1111/j.1365-2486.2010.02368.x DOI

Walker M., Pérez M., Steinbrecher T., Gawthrop F., Pavlovic I., Novák O., et al. . (2021). Molecular mechanisms and hormonal regulation underpinning morphological dormancy: a case study using Apium graveolens (Apiaceae). Plant J. 108, 1020–1036. doi: 10.1111/tpj.15489 PubMed DOI

Wang L., Huang Z., Baskin C. C., Baskin J. M., Dong M. (2008). Germination of dimorphic seeds of the desert annual halophyte Suaeda aralocaspica (Chenopodiaceae), a C4 plant without kranz anatomy. Ann. Bot. 102, 757–769. doi: 10.1093/aob/mcn158 PubMed DOI PMC

Wang F., Xu Y. G., Wang S., Shi W., Liu R., Feng G., et al. . (2015). Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa . Plant Physiol. Biochem. 95, 41–48. doi: 10.1016/j.plaphy.2015.07.005 PubMed DOI

Westwood J. H., Charudattan R., Duke S. O., Fennimore S. A., Marrone P., Slaughter D. C., et al. . (2018). Weed management in 2050: Perspectives on the future of weed science. Weed Sci. 66, 275–285. doi: 10.1017/wsc.2017.78 DOI

Wu Q., Bai X., Wu X. Y., Xiang D. B., Wan Y., Luo Y. M., et al. . (2020). Transcriptome profiling identifies transcription factors and key homologs involved in seed dormancy and germination regulation of Chenopodium quinoa . Plant Physiol. Biochem. 151, 443–456. doi: 10.1016/j.plaphy.2020.03.050 PubMed DOI

Xu Y., Zhao Y., Duan H., Sui N., Yuan F., Song J. (2017). Transcriptomic profiling of genes in matured dimorphic seeds of euhalophyte Suaeda salsa . BMC Genomics 18, 727. doi: 10.1186/s12864-017-4104-9 PubMed DOI PMC

Yao S., Lan H., Zhang F. (2010). Variation of seed heteromorphism in Chenopodium album and the effect of salinity stress on the descendants. Ann. Bot. 105, 1015–1025. doi: 10.1093/aob/mcq060 PubMed DOI PMC

Zeller R. (2001). Fixation, embedding, and sectioning of tissues, embryos, and single cells. Curr. Protoc. Pharmacol. 7, A.3D.1–A.3D.9. doi: 10.1002/0471141755.pha03ds07 PubMed DOI

Zhao S., Fernald R. D. (2005). Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 12, 1047–1064. doi: 10.1089/cmb.2005.12.1047 PubMed DOI PMC

Zheng Y., Huang Y. Y., Xian W. H., Wang J. X., Liao H. (2012). Identification and expression analysis of the Glycine max CYP707A gene family in response to drought and salt stresses. Ann. Bot. 110, 743–756. doi: 10.1093/aob/mcs133 PubMed DOI PMC

The dimorphic diaspore model Aethionema arabicum (Brassicaceae): Distinct molecular and morphological control of responses to parental and germination temperatures

Aethionema arabicum dimorphic seed trait resetting during transition to seedlings