Developmental Control and Plasticity of Fruit and Seed Dimorphism in Aethionema arabicum
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
I 1477
Austrian Science Fund FWF - Austria
BB/M00192X/1
Biotechnology and Biological Sciences Research Council - United Kingdom
BB/M000583/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
27702842
PubMed Central
PMC5100781
DOI
10.1104/pp.16.00838
PII: pp.16.00838
Knihovny.cz E-zdroje
- MeSH
- biologické modely MeSH
- Brassicaceae anatomie a histologie embryologie genetika ultrastruktura MeSH
- down regulace genetika MeSH
- fenotyp MeSH
- fylogeneze MeSH
- klíčení genetika MeSH
- ovoce embryologie genetika ultrastruktura MeSH
- regulace genové exprese u rostlin MeSH
- rostlinné geny MeSH
- rostlinné proteiny genetika metabolismus MeSH
- sekvenční homologie aminokyselin MeSH
- semena rostlinná embryologie genetika ultrastruktura MeSH
- šíření semen MeSH
- vývojová regulace genové exprese MeSH
- vývojové geny MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- rostlinné proteiny MeSH
Understanding how plants cope with changing habitats is a timely and important topic in plant research. Phenotypic plasticity describes the capability of a genotype to produce different phenotypes when exposed to different environmental conditions. In contrast, the constant production of a set of distinct phenotypes by one genotype mediates bet hedging, a strategy that reduces the temporal variance in fitness at the expense of a lowered arithmetic mean fitness. Both phenomena are thought to represent important adaptation strategies to unstable environments. However, little is known about the underlying mechanisms of these phenomena, partly due to the lack of suitable model systems. We used phylogenetic and comparative analyses of fruit and seed anatomy, biomechanics, physiology, and environmental responses to study fruit and seed heteromorphism, a typical morphological basis of a bet-hedging strategy of plants, in the annual Brassicaceae species Aethionema arabicum Our results indicate that heteromorphism evolved twice within the Aethionemeae, including once for the monophyletic annual Aethionema clade. The dimorphism of Ae. arabicum is associated with several anatomic, biomechanical, gene expression, and physiological differences between the fruit and seed morphs. However, fruit ratios and numbers change in response to different environmental conditions. Therefore, the life-history strategy of Ae. arabicum appears to be a blend of bet hedging and plasticity. Together with the available genomic resources, our results pave the way to use this species in future studies intended to unravel the molecular control of heteromorphism and plasticity.
Biosystematics Group Wageningen University 6708 PB Wageningen The Netherlands ; and
Department of Biology Botany University of Osnabrück 49076 Osnabrueck Germany
Department of Biology Botany University of Osnabrück 49076 Osnabrueck Germany ;
Department of Biology Science Faculty Gazi University 06500 Teknikokullar Ankara Turkey
Department of Biology Science Faculty Gazi University 06500 Teknikokullar Ankara Turkey ;
Department of Botany Faculty of Science Hacettepe University 06800 Beytepe Ankara Turkey
Department of Botany Faculty of Science Hacettepe University 06800 Beytepe Ankara Turkey ;
Department of Genetics Friedrich Schiller University 07743 Jena Germany
Department of Genetics Friedrich Schiller University 07743 Jena Germany ;
Department of Physiology Faculty of Medicine Mersin University 33343 Mersin Turkey
Department of Physiology Faculty of Medicine Mersin University 33343 Mersin Turkey ;
Plant Cell Biology Faculty of Biology University of Marburg 35043 Marburg Germany
Plant Cell Biology Faculty of Biology University of Marburg 35043 Marburg Germany ;
Zobrazit více v PubMed
Abley K, Locke JCW, Leyser HMO (2016) Developmental mechanisms underlying variable, invariant and plastic phenotypes. Ann Bot (Lond) 117: 733–748 PubMed PMC
Al-Shehbaz IA. (2012) A generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon 61: 931–954
Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Syst Evol 259: 89–120
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410 PubMed
Andersson I, Carlström A, Franzén R, Karlén T, Nybom H (1983) A revision of the Aethionema saxatile complex (Brassicaceae). Willdenowia 13: 3–42
Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, Sablowski R, Østergaard L (2010) Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev 24: 2127–2132 PubMed PMC
Arnaud N, Lawrenson T, Østergaard L, Sablowski R (2011) The same regulatory point mutation changed seed-dispersal structures in evolution and domestication. Curr Biol 21: 1215–1219 PubMed
Avino M, Kramer EM, Donohue K, Hammel AJ, Hall JC (2012) Understanding the basis of a novel fruit type in Brassicaceae: conservation and deviation in expression patterns of six genes. Evodevo 3: 20. PubMed PMC
Bakker FT, Lei D, Yu J, Mohammadin S, Wei Z, Kerke S, Gravendeel B, Nieuwenhuis M, Staats M, Alquezar‐Planas DE (2016) Herbarium genomics: plastome sequence assembly from a range of herbarium specimens using an Iterative Organelle Genome Assembly pipeline. Biol J Linn Soc Lond 117: 33–43
Baskin JM, Lu JJ, Baskin CC, Tan DY, Wang L (2014) Diaspore dispersal ability and degree of dormancy in heteromorphic species of cold deserts of northwest China: a review. Perspect Plant Ecol Evol Syst 16: 93–99
Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci USA 107: 18724–18728 PubMed PMC
Bradford MJ, Roff DA (1993) Bet hedging and the diapause strategies of the cricket Allonemobius fasciatus. Ecology 74: 1129–1135
Clamp M, Cuff J, Searle SM, Barton GJ (2004) The Jalview Java alignment editor. Bioinformatics 20: 426–427 PubMed
Cruz-Mazo G, Buide ML, Samuel R, Narbona E (2009) Molecular phylogeny of Scorzoneroides (Asteraceae): evolution of heterocarpy and annual habit in unpredictable environments. Mol Phylogenet Evol 53: 835–847 PubMed
Dinneny JR, Weigel D, Yanofsky MF (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development 132: 4687–4696 PubMed
Donohue K, Rubio de Casas R, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41: 293–319
Dubois J, Cheptou PO (2012) Competition/colonization syndrome mediated by early germination in non-dispersing achenes in the heteromorphic species Crepis sancta. Ann Bot (Lond) 110: 1245–1251 PubMed PMC
Dumolin-Lapegue S, Pemonge MH, Petit RJ (1997) An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol 6: 393–397 PubMed
Estornell LH, Agustí J, Merelo P, Talón M, Tadeo FR (2013) Elucidating mechanisms underlying organ abscission. Plant Sci 199-200: 48–60 PubMed
Evans MEK, Dennehy JJ (2005) Germ banking: bet-hedging and variable release from egg and seed dormancy. Q Rev Biol 80: 431–451 PubMed
Fernández IA, Aguilar JF, Panero JL, Feliner GN (2001) A phylogenetic analysis of Doronicum (Asteraceae, Senecioneae) based on morphological, nuclear ribosomal (ITS), and chloroplast (trnL-F) evidence. Mol Phylogenet Evol 20: 41–64 PubMed
Ferrandiz C. (2011) Fruit structure and diversity. eLS doi/10.1002/9780470015902.a0002044.pub2
Ferrándiz C, Liljegren SJ, Yanofsky MF (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289: 436–438 PubMed
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171: 501–523 PubMed
Fofana B, Harvengt L, Baudoin JP, Du Jardin P (1997) New primers for the polymerase chain amplification of cpDNA intergenic spacers in Phaseolus phylogeny. Belg J Bot 129: 118–122
Francoz E, Ranocha P, Burlat V, Dunand C (2015) Arabidopsis seed mucilage secretory cells: regulation and dynamics. Trends Plant Sci 20: 515–524 PubMed
Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K (2011) Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci 16: 108–116 PubMed
Frickenhaus S, Beszteri B (2008) Quicktree-SD. AWI Bioinformatics, Bremerhaven, Germany, http://hdl.handle.net/10013/epic.33164.d001
Gerlach D. (1984) Botanische Mikrotechnik, eine Einführung, 2. Georg Thieme Verlag, Stuttgart, Germany
Gilbert SF, Bosch TC, Ledón-Rettig C (2015) Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat Rev Genet 16: 611–622 PubMed
Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJJ (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ 35: 1769–1786 PubMed
Greenspan L. (1977) Humidity fixed points of binary saturated aqueous solutions. J Res Natl Bur Stand 81: 89–96
Groszmann M, Paicu T, Alvarez JP, Swain SM, Smyth DR (2011) SPATULA and ALCATRAZ, are partially redundant, functionally diverging bHLH genes required for Arabidopsis gynoecium and fruit development. Plant J 68: 816–829 PubMed
Gutterman Y. (1993) Seed Germination in Desert Plants: Adaptation of Desert Organisms. Springer-Verlag, Berlin
Gutterman Y. (2012) Survival Strategies of Annual Desert Plants. Springer, New York, NY
Hall JC, Tisdale TE, Donohue K, Kramer EM (2006) Developmental basis of an anatomical novelty: heteroarthrocarpy in Cakile lanceolata and Erucaria erucarioides (Brassicaceae). Int J Plant Sci 167: 771–789
Haudry A, Platts AE, Vello E, Hoen DR, Leclercq M, Williamson RJ, Forczek E, Joly-Lopez Z, Steffen JG, Hazzouri KM, et al. (2013) An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat Genet 45: 891–898 PubMed
Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci 10: 472–477 PubMed
Hedge IC. (1965) Aethionema R. Br. In Davis PH, ed, Flora of Turkey and the East Aegean Islands, Vol 1 University Press, Edinburgh, UK, pp 314–332
Hofberger JA, Nsibo DL, Govers F, Bouwmeester K, Schranz ME (2015) A complex interplay of tandem- and whole-genome duplication drives expansion of the L-type lectin receptor kinase gene family in the Brassicaceae. Genome Biol Evol 7: 720–734 PubMed PMC
Howe K, Bateman A, Durbin R (2002) QuickTree: building huge neighbour-joining trees of protein sequences. Bioinformatics 18: 1546–1547 PubMed
Huang Y, Shi S (2002) Phylogenetics of Lythraceae sensu lato: a preliminary analysis based on chloroplast rbcL gene, psaA‐ycf3 spacer, and nuclear rDNA internal transcribed spacer (ITS) sequences. Int J Plant Sci 163: 215–225
Huang Z, Zhenghai H, Zhenghai H, Huang Z, Gutterman Y (2000) Structure and function of mucilaginous achenes of Artemisia monosperma inhabiting the Negev Desert of Israel. Isr J Plant Sci 48: 255–266
Imbert E. (2002) Ecological consequences and ontogeny of seed heteromorphism. Perspect Plant Ecol Evol Syst 5: 13–36
Imbert E, Ronce O (2001) Phenotypic plasticity for dispersal ability in the seed heteromorphic Crepissancta (Asteraceae). Oikos 93: 126–134
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780 PubMed PMC
Khosravi AR, Jacquemoud F, Mohsenzadeh S, Menke M, Mummenhoff K (2009) Phylogenetic position and taxonomic classification of Aethionema trinervium (Brassicaceae): a morphologically variable subshrub from southwestern Asia 1. Ann Mo Bot Gard 96: 564–574
Kunieda T, Mitsuda N, Ohme-Takagi M, Takeda S, Aida M, Tasaka M, Kondo M, Nishimura M, Hara-Nishimura I (2008) NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. Plant Cell 20: 2631–2642 PubMed PMC
Lee KJ, Dekkers BJ, Steinbrecher T, Walsh CT, Bacic A, Bentsink L, Leubner-Metzger G, Knox JP (2012) Distinct cell wall architectures in seed endosperms in representatives of the Brassicaceae and Solanaceae. Plant Physiol 160: 1551–1566 PubMed PMC
Lenser T, Theißen G (2014) Quantifying fruit dehiscence using the random impact test (RIT). Bio Protoc 4: e1200
Li C, Zhou A, Sang T (2006) Rice domestication by reducing shattering. Science 311: 1936–1939 PubMed
Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766–770 PubMed
Liljegren SJ, Roeder AHK, Kempin SA, Gremski K, Østergaard L, Guimil S, Reyes DK, Yanofsky MF (2004) Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116: 843–853 PubMed
Linkies A, Graeber K, Knight C, Leubner-Metzger G (2010) The evolution of seeds. New Phytol 186: 817–831 PubMed
Lu J, Tan D, Baskin JM, Baskin CC (2010) Fruit and seed heteromorphism in the cold desert annual ephemeral Diptychocarpus strictus (Brassicaceae) and possible adaptive significance. Ann Bot (Lond) 105: 999–1014 PubMed PMC
Lu JJ, Ma WB, Tan DY, Baskin JM, Baskin CC (2013a) Effects of environmental stress and nutlet morph on proportion and within-flower number-combination of morphs produced by the fruit-dimorphic species Lappula duplicicarpa (Boraginaceae). Plant Ecol 214: 351–362
Lu JJ, Tan DY, Baskin JM, Baskin CC (2012) Phenotypic plasticity and bet-hedging in a heterocarpic winter annual/spring ephemeral cold desert species of Brassicaceae. Oikos 121: 357–366
Lu JJ, Tan DY, Baskin JM, Baskin CC (2013b) Trade-offs between seed dispersal and dormancy in an amphi-basicarpic cold desert annual. Ann Bot (Lond) 112: 1815–1827 PubMed PMC
Lu JJ, Tan DY, Baskin JM, Baskin CC (2014) Germination season and watering regime, but not seed morph, affect life history traits in a cold desert diaspore-heteromorphic annual. PLoS ONE 9: e102018. PubMed PMC
Lu JJ, Tan DY, Baskin JM, Baskin CC (2015) Post-release fates of seeds in dehiscent and indehiscent siliques of the diaspore heteromorphic species Diptychocarpus strictus (Brassicaceae). Perspect Plant Ecol Evol Syst 17: 255–262
Mandák B, Pyšek P (1999) Effects of plant density and nutrient levels on fruit polymorphism in Atriplex sagittata. Oecologia 119: 63–72 PubMed
Mandak B, Pysek P (2001) Fruit dispersal and seed banks in Atriplex sagittata: the role of heterocarpy. J Ecol 89: 159–165
Matilla A, Gallardo M, Puga-Hermida MI (2005) Structural, physiological and molecular aspects of heterogeneity in seeds: a review. Seed Sci Res 15: 63–76
Meakin PJ, Roberts JA (1990a) Dehiscence of fruit in oilseed rape (Brassica napus L.). 1. Anatomy of pod dehiscence. J Exp Bot 41: 995–1002
Meakin PJ, Roberts JA (1990b) Dehiscence of fruit in oilseed rape (Brassica napus L.). 2. The role of cell-wall degrading enzymes and ethylene. J Exp Bot 41: 1003–1011
Mohammadin S, Edger PP, Pires JC, Schranz ME (2015) Positionally-conserved but sequence-diverged: identification of long non-coding RNAs in the Brassicaceae and Cleomaceae. BMC Plant Biol 15: 217. PubMed PMC
Mühlhausen A, Lenser T, Mummenhoff K, Theißen G (2013) Evidence that an evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae) was caused by a change in the control of valve margin identity genes. Plant J 73: 824–835 PubMed
Mühlhausen A, Polster A, Theißen G, Mummenhoff K (2010) Evolution of fruit dehiscence in Brassicaceae: examples from Aethionema and Lepidium. Acta Hortic 867: 207–219
Müller K, Tintelnot S, Leubner-Metzger G (2006) Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol 47: 864–877 PubMed
Mummenhoff K, Franzke A (2007) Gone with the bird: late tertiary and quaternary intercontinental long‐distance dispersal and allopolyploidization in plants. Syst Biodivers 5: 255–260
Norton DA, Delange PJ, Garnock-Jones PJ, Given DR (1997) The role of seabirds and seals in the survival of coastal plants: lessons from New Zealand Lepidium (Brassicaceae). Biodivers Conserv 6: 765–785
Østergaard L, Kempin SA, Bies D, Klee HJ, Yanofsky MF (2006) Pod shatter-resistant Brassica fruit produced by ectopic expression of the FRUITFULL gene. Plant Biotechnol J 4: 45–51 PubMed
Parolin P. (2006) Ombrohydrochory: rain-operated seed dispersal in plants—with special regard to jet-action dispersal in Aizoaceae. Flora 201: 511–518
Philippi T, Seger J (1989) Hedging one’s evolutionary bets, revisited. Trends Ecol Evol 4: 41–44 PubMed
Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209: 2362–2367 PubMed
Pufal G, Garnock-Jones P (2010) Hygrochastic capsule dehiscence supports safe site strategies in New Zealand alpine Veronica (Plantaginaceae). Ann Bot (Lond) 106: 405–412 PubMed PMC
Rajani S, Sundaresan V (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol 11: 1914–1922 PubMed
Ripoll JJ, Roeder AH, Ditta GS, Yanofsky MF (2011) A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development 138: 5167–5176 PubMed
Rost B. (1999) Twilight zone of protein sequence alignments. Protein Eng 12: 85–94 PubMed
Rubio de Casas R, Donohue K, Venable DL, Cheptou PO (2015) Gene-flow through space and time: dispersal, dormancy and adaptation to changing environments. Evol Ecol 29: 813–831
Sadeh A, Guterman H, Gersani M, Ovadia O (2009) Plastic bet-hedging in an amphicarpic annual: an integrated strategy under variable conditions. Evol Ecol 23: 373–388
Schranz ME, Mohammadin S, Edger PP (2012) Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model. Curr Opin Plant Biol 15: 147–153 PubMed
Scutt CP, Vinauger-Douard M, Fourquin C, Finet C, Dumas C (2006) An evolutionary perspective on the regulation of carpel development. J Exp Bot 57: 2143–2152 PubMed
Seymour G, Poole M, Manning K, King GJ (2008) Genetics and epigenetics of fruit development and ripening. Curr Opin Plant Biol 11: 58–63 PubMed
Simon S, Rühl M, de Montaigu A, Wötzel S, Coupland G (2015) Evolution of CONSTANS regulation and function after gene duplication produced a photoperiodic flowering switch in the Brassicaceae. Mol Biol Evol 32: 2284–2301 PubMed PMC
Simons AM. (2011) Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proc Biol Sci 278: 1601–1609 PubMed PMC
Solms-Laubach HG (1901) Über die Arten des Genus Aethionema, die Schließfrüchte hervorbringen. In Botanische Zeitung. Verlag von Arthur Felix, Leipzig, Germany, pp 61–78
Sorensen AE. (1986) Seed dispersal by adhesion. Annu Rev Ecol Syst 17: 443–463
Spence J, Vercher Y, Gates P, Harris N (1996) ‘Pod shatter’ in Arabidopsis thaliana, Brassica napus and B. juncea. J Microsc 181: 195–203
Sultan SE. (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5: 537–542 PubMed
Takeno K, Yamaguchi H (1991) Diversity in seed germination behavior in relation to heterocarpy in Salsola komarovii Iljin. Bot Mag Tokyo 104: 207–215
Venable DL. (2007) Bet hedging in a guild of desert annuals. Ecology 88: 1086–1090 PubMed
Venable DL, Dyreson E, Morlaes E (1995) Population dynamic consequences and evolution of seed traits of Heterosperma pinnatum (Asteraceae). Am J Bot 82: 410–420
Venable DL, Lawlor L (1980) Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia 46: 272–282 PubMed
Venable DL, Levin DA (1985) Ecology of achene dimorphism in Heterotheca latifolia. 1. Achene structure, germination and dispersal. J Ecol 73: 133–145
Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10: 212–217 PubMed
Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62: 3289–3309 PubMed
Western TL. (2012) The sticky tale of seed coat mucilages: production, genetics, and role in seed germination and dispersal. Seed Sci Res 22: 1–25
Western TL, Burn J, Tan WL, Skinner DJ, Martin-McCaffrey L, Moffatt BA, Haughn GW (2001) Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol 127: 998–1011 PubMed PMC
Yang F, Baskin JM, Baskin CC, Yang X, Cao D, Huang Z (2015) Effects of germination time on seed morph ratio in a seed-dimorphic species and possible ecological significance. Ann Bot (Lond) 115: 137–145 PubMed PMC
Yang X, Baskin JM, Baskin CC, Huang Z (2012) More than just a coating: ecological importance, taxonomic occurrence and phylogenetic relationships of seed coat mucilage. Perspect Plant Ecol Evol Syst 14: 434–442
Yang X, Dong M, Huang Z (2010) Role of mucilage in the germination of Artemisia sphaerocephala (Asteraceae) achenes exposed to osmotic stress and salinity. Plant Physiol Biochem 48: 131–135 PubMed
Yang X, Zhang W, Dong M, Boubriak I, Huang Z (2011) The achene mucilage hydrated in desert dew assists seed cells in maintaining DNA integrity: adaptive strategy of desert plant Artemisia sphaerocephala. PLoS ONE 6: e24346. PubMed PMC
Zohary M. (1962) Plant Life of Palestine: Israel and Jordan. Ronald Press Company, New York, NY
Zohary M, Fahn A (1950) On the heterocarpy of Aethionema. Palestine J Bot 5: 28–31
Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
Genomic Blocks in Aethionema arabicum Support Arabideae as Next Diverging Clade in Brassicaceae
Aethionema arabicum: a novel model plant to study the light control of seed germination