The origin of the agriculture was one of the turning points in human history, and a central part of this was the evolution of new plant forms, domesticated crops. Seed dispersal and germination are two key traits which have been selected to facilitate cultivation and harvesting of crops. The objective of this study was to analyze anatomical structure of seed coat and pod, identify metabolic compounds associated with water-impermeable seed coat and differentially expressed genes involved in pea seed dormancy and pod dehiscence. Comparative anatomical, metabolomics, and transcriptomic analyses were carried out on wild dormant, dehiscent Pisum elatius (JI64, VIR320) and cultivated, indehiscent Pisum sativum non-dormant (JI92, Cameor) and recombinant inbred lines (RILs). Considerable differences were found in texture of testa surface, length of macrosclereids, and seed coat thickness. Histochemical and biochemical analyses indicated genotype related variation in composition and heterogeneity of seed coat cell walls within macrosclereids. Liquid chromatography-electrospray ionization/mass spectrometry and Laser desorption/ionization-mass spectrometry of separated seed coats revealed significantly higher contents of proanthocyanidins (dimer and trimer of gallocatechin), quercetin, and myricetin rhamnosides and hydroxylated fatty acids in dormant compared to non-dormant genotypes. Bulk Segregant Analysis coupled to high throughput RNA sequencing resulted in identification of 770 and 148 differentially expressed genes between dormant and non-dormant seeds or dehiscent and indehiscent pods, respectively. The expression of 14 selected dormancy-related genes was studied by qRT-PCR. Of these, expression pattern of four genes: porin (MACE-S082), peroxisomal membrane PEX14-like protein (MACE-S108), 4-coumarate CoA ligase (MACE-S131), and UDP-glucosyl transferase (MACE-S139) was in agreement in all four genotypes with Massive analysis of cDNA Ends (MACE) data. In case of pod dehiscence, the analysis of two candidate genes (SHATTERING and SHATTERPROOF) and three out of 20 MACE identified genes (MACE-P004, MACE-P013, MACE-P015) showed down-expression in dorsal and ventral pod suture of indehiscent genotypes. Moreover, MACE-P015, the homolog of peptidoglycan-binding domain or proline-rich extensin-like protein mapped correctly to predicted Dpo1 locus on PsLGIII. This integrated analysis of the seed coat in wild and cultivated pea provides new insight as well as raises new questions associated with domestication and seed dormancy and pod dehiscence.

Agricultural Research Ltd Troubsko Czechia

Department of Analytical Chemistry Regional Centre of Advanced Technologies and Materials Palacký University in OlomoucOlomouc Czechia

Department of Botany Palacký University in OlomoucOlomouc Czechia

Department of Crop Science Breeding and Plant Medicine Mendel University in BrnoBrno Czechia

Department of Experimental Plant Biology Charles UniversityPrague Czechia

Department of Plant Biology Mendel University in BrnoBrno Czechia

Faculty of Science Palacký University in OlomoucOlomouc Czechia

GenXProFrankfurt Germany

Research Program Genetic Gains ICRISATHyderabad India

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Abbo S., Rachamim E., Zehavi Y., Zezak I., Lev-Yadun S., Gopher A. (2011). Experimental growing of wild pea in Israel and its bearing on near Eastern plant domestication. Ann. Bot. 107, 1399–1404. 10.1093/aob/mcr081 PubMed DOI PMC

Agati G., Azzarello E., Pollastri S., Tattini M. (2012). Flavonoids as antioxidants in plants: location and functional significance. Plant Sci. 196, 67–76. 10.1016/j.plantsci.2012.07.014 PubMed DOI

Agbo G. N., Hosfield M. A., Uebersax M. A., Klomparens K. (1987). Seed microstructure and its relationship to water uptake in isogenic lines and a cultivar of drybeans (Phaseolus vulgaris L.). Food Microstruct. 6, 91–102.

Aghamirzaie D., Batra D., Heath L. S., Schneider A., Grene R., Collakova E. (2015). Transcriptome-wide functional characterization reveals novel relationships among differentially expressed transcripts in developing soybean embryos. BMC Genomics 16:928. 10.1186/s12864-015-2108-x PubMed DOI PMC

Alves-Carvalho S., Aubert G., Carrere S., Cruaud C., Brochot A.-L., Jacquin F., et al. (2015). Full-lenght de novo assembly of RNAseq data in pea (Pisum sativum L.) provides a gene expression atlas and gives insights in root nodulation in this species. Plant J. 8, 1–19. 10.1111/tpj.12967 PubMed DOI

Amarowicz R., Estrella I., Hernández T., Dueñas M., Troszyńska A., Kosińska A., et al. . (2009). Antioxidant activity of a red lentil extract and its fractions. Int. J. Mol. Sci. 10, 5513–5527. 10.3390/ijms10125513 PubMed DOI PMC

Ambrose M. J., Ellis T. H. N. (2008). Ballistic seed dispersal and associated seed shadow in wild Pisum germplasm. Pisum Genet. 40, 5–10.

Appelhagen I., Thiedig K., Nordholt N., Schmidt N., Huep G., Sagasser M., et al. . (2014). Update on transparent testa mutants from Arabidopsis thaliana: characterisation of new alleles from an isogenic collection. Planta 240, 955–970. 10.1007/s00425-014-2088-0 PubMed DOI

Armon S., Efrati E., Kupferman R., Sharon E. (2011). Geometry and mechanics in the opening of chiral seed pods. Science 333, 1726–1730. 10.1126/science.1203874 PubMed DOI

Bajaj D., Das S., Upadhyaya H. D., Ranjan R., Badoni S., Kumar V., et al. . (2015). A genome-wide combinatorial strategy dissects complex genetic architecture of seed coat color in chickpea. Front. Plant Sci. 6:979. 10.3389/fpls.2015.00979 PubMed DOI PMC

Ballester P., Ferrandiz C. (2016). Shattering fruits: variations on a dehiscent theme. Curr. Opin. Plant Biol. 35, 68–75. 10.1016/j.pbi.2016.11.008 PubMed DOI

Barros E., Lezar S., Anttonen M. J., van Dijk J. P., Röhlig R. M., Kok E. J., et al. . (2010). Comparison of two GM maize varieties with a near-isogenic non-GM variety using transcriptomics, proteomics and metabolomics. Plant Biotechnol. J. 8, 436–451. 10.1111/j.1467-7652.2009.00487.x PubMed DOI

Baskin J. M., Baskin C. C. (2004). A classification system for seed dormancy. Seed Sci. Res. 14, 1–16. 10.1079/SSR2003150 DOI

Baskin J. M., Baskin C. C., Li X. (2000). Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biol. 15, 139–152. 10.1046/j.1442-1984.2000.00034.x DOI

Beisson F., Li Y., Bonaventure G., Pollard M., Ohlrogge J. B. (2007). The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19, 351–368. 10.1105/tpc.106.048033 PubMed DOI PMC

Benedito V. A., Torres-Jerez I., Murray J. D., Andriankaja A., Allen S., Kakar K., et al. . (2008). A gene expression atlas of the model legume Medicago truncatula. Plant J. 55, 504–513. 10.1111/j.1365-313X.2008.03519.x PubMed DOI

Bennett E. J., Roberts J. A., Wagstaff C. (2011). The role of the pod in seed development: strategies for manipulating yield. New Phytol. 190, 838–853. 10.1111/j.1469-8137.2011.03714.x PubMed DOI

Bewley J. D. (1997). Seed germination and dormancy. Plant Cell 9, 1055–1066. 10.1105/tpc.9.7.1055 PubMed DOI PMC

Bewley J. D., Bradford K., Hilhorst H., Nonogaki H. (2013). Seeds: Physiology of Development, Germination and Dormancy, 3rd Edn. NewYork, NY: Springer-Verlag; 10.1007/978-1-4614-4693-4 DOI

Bogdanova V. S., Galieva E. R., Yadrikhinskiy A. K., Kosterin O. E. (2012). Inheritance and genetic mapping of two nuclear genes involved in nuclear–cytoplasmic incompatibility in peas (Pisum sativum L.). Theor. Appl. Genet. 124, 1503–1512. 10.1007/s00122-012-1804-z PubMed DOI

Bojahr J., Nhengiwa O., Krezdorn N., Rotter B., Saal B., Ruge-Wehling B., et al. . (2016). Massive analysis of cDNA ends (MACE) reveals a co-segregating candidate gene for LpPg1 stem rust resistance in perennial ryegrass (Lolium perenne). Theor. Appl. Genet. 129, 1915–1932. 10.1007/s00122-016-2749-4 PubMed DOI

Bordat A., Savois V., Nicolas M., Salse J., Chauveau A., Bourgeois M., et al. . (2011). Translational genomics in legumes allowed placing in silico 5460 unigenes on the pea functional map and identified candidate genes in Pisum sativum L. G3 1, 93–103. 10.1534/g3.111.000349 PubMed DOI PMC

Bradford K., Nonogaki H. (2009). Seed Development, Dormancy and Germination. Annual Plant Review, Vol. 27 Oxford: Blackwell.

Caldas G. V., Blair M. W. (2009). Inheritance of condensed tannin content and relationship with seed colour and pattern genes in common bean (Phaseolus vulgaris L.). Theor. Appl. Genet. 119, 131–142. 10.1007/s00122-009-1023-4 PubMed DOI

Chai M., Zhou C., Molina I., Fu C., Nakashima J., Li G., et al. . (2016). A class II KNOX gene, KNOX4, controls seed physical dormancy. Proc. Natl. Acad. Sci. U.S.A. 113, 6997–7002. 10.1073/pnas.1601256113 PubMed DOI PMC

Chayut N., Yuan H., Ohali S., Meir A., Yeselson Y., Portnoy V., et al. . (2015). A bulk segregant transcriptome analysis reveals metabolic and cellular processes associated with Orange allelic variation and fruit β-carotene accumulation in melon fruit. BMC Plant Biol. 15:274. 10.1186/s12870-015-0661-8 PubMed DOI PMC

Chen H., Osuna D., Colville L., Lorenzo O., Graeber K., Küster H., et al. . (2013). Transcriptome-wide mapping of pea seed ageing reveals a pivotal role for genes related to oxidative stress and programmed cell death. PLoS ONE 8:e78471. 10.1371/journal.pone.0078471 PubMed DOI PMC

Chomczynski P., Sacchi N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156–159. PubMed

Christiansen L. C., Dal Degan F., Ulvskov P., Borkhardt B. (2002). Examination of the dehiscence zone in soybean pods and isolation of a dehiscence-related endopolygalacturonase gene. Plant Cell Environ. 25, 479–490. 10.1046/j.1365-3040.2002.00839.x DOI

Collakova E., Aghamirzaie D., Fang Y., Klumas C., Tabataba F., Kakumanu A., et al. . (2013). Metabolic and transcriptional reprogramming in developing soybean (Glycine max) embryos. Metabolites 3, 347–372. 10.3390/metabo3020347 PubMed DOI PMC

de Souza F. H. D., Marcos-Filho J. (2001). A seed coat as a modulator of seed-environment relationships in Fabaceae. Rev. Bras. Bot. 24, 365–375. 10.1590/s0100-84042001000400002 DOI

de Souza T. V., Voltolini C. H., Santos M., Silveira Paulilo M. T. (2012). Water absorption and dormancy-breaking requirements of physically dormant seeds of Schizolobium parahyba (Fabaceae–Caesalpinioideae). Seed Sci. Res. 22, 169–176. 10.1017/S0960258512000013 DOI

Debeaujon I., Léon-Kloosterziel K. M., Koornneef M. (2000). Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol. 122, 403–414. 10.1104/pp.122.2.403 PubMed DOI PMC

Dixon R. A., Sharma S. B., Xie D. (2005). Proanthocyanidins—a final frontier in flavonoid research? New Phytol. 165, 9–28. 10.1111/j.1469-8137.2004.01217.x PubMed DOI

Doebley J., Stec A., Hubbard L. (1997). The evolution of apical dominance in maize. Nature 386, 485–488. 10.1038/386485a0 PubMed DOI

Dong Y., Wang Y.-Z. (2015). Seed shattering: from models to crops. Front. Plant Sci. 6:476. 10.3389/fpls.2015.00476 PubMed DOI PMC

Dong Y., Yang X., Liu J., Wang B. H., Liu B. L., Wang Y. Z., et al. . (2014). Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean. Nat. Commun. 5:3352. 10.1038/ncomms4352 PubMed DOI

Duarte J., Riviere N., Baranger A., Aubert G., Burstin J., Cornet L., et al. . (2014). Transcriptome sequencing for high throughput SNP development and genetic mapping in pea. BMC Genomics 15:126. 10.1186/1471-2164-15-126 PubMed DOI PMC

Dueñas M., Estrella I., Hernández T. (2004). Occurrence of phenolic compounds in the seed coat and the cotyledon of peas (Pisum sativum L.). Eur. Food Res. Technol. 219, 116–123. 10.1007/s00217-004-0938-x DOI

Enfissi E. M., Barneche F., Ahmed I., Lichtlé C., Gerrish C., McQuinm R. P., et al. . (2010). Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22, 1190–1215. 10.1105/tpc.110.073866 PubMed DOI PMC

Evans N. A., Hoyne P. A., Stone B. A. (1984). Characteristics and specificity of the interaction of a fluorochrome from aniline blue (sirofluor) with polysaccharides. Carbohydr. Polym. 4, 215–230. 10.1016/0144-8617(84)90012-2 DOI

Ferrándiz C., Liljegren S. J., Yanofsky M. F. (2000). Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289, 436–438. 10.1126/science.289.5478.436 PubMed DOI

Ferraro K., Jin A. L., Nguyen T.-R., Reinecke D. M., Ozga J. A., Ro D.-K. (2014). Characterization of proanthocyanidin metabolism in pea (Pisum sativum) seeds. BMC Plant Biol. 14:238. 10.1186/s12870-014-0238-y PubMed DOI PMC

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

Foyer C. H., Lam H. M., Nguyen H. T., Siddique K. H. M., Varshney R. K., Colmer T. D., et al. . (2016). Neglecting legumes has compromised human health and sustainable food production. Nature Plants 2, 1–10. 10.1038/nplants.2016.112 PubMed DOI

Franssen S. U., Shrestha R. P., Bräutigam A., Bornberg-Bauer E., Weber A. P. (2011). Comprehensive transcriptome analysis of the highly complex Pisum sativum genome using next generation sequencing. BMC Genomics 12:227. 10.1186/1471-2164-12-227 PubMed DOI PMC

Fuller D. Q., Allaby R. G. (2009). Seed dispersal and crop domestication: shattering, germination and seasonality in evolution under cultivation. Ann. Plant Rev. 38, 238–295. 10.1002/9781444314557.ch7 DOI

Fuller D. Q., Denham T., Arroyo-Kalin M., Lucas M., Stevens C. J., Qin L., et al. . (2014). Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record. Proc. Natl. Acad. Sci. U.S.A. 111, 6147–6152. 10.1073/pnas.1308937110 PubMed DOI PMC

Funatsuki H., Suzuki M., Hirose A., Inaba H., Yamada T., Hajika M., et al. . (2014). Molecular basis of a shattering resistance boosting global dissemination of soybean. Proc. Natl. Acad. Sci. U.S.A. 111, 17797–17802. 10.1073/pnas.1417282111 PubMed DOI PMC

Gallardo K., Firnhaber C., Zuber H., Héricher D., Belghazi M., Henry C., et al. . (2007). A combined proteome and transcriptome analysis of developing Medicago truncatula seeds. Mol. Cell. Proteomics 6, 2165–2179. 10.1074/mcp.M700171-MCP200 PubMed DOI

Gardner R. O. (1975). Vanillin - hydrochloric acid as a histochemical test for tannin. Stain Technol. 50, 315–317. 10.3109/10520297509117081 PubMed DOI

Gillikin J. W., Graham J. S. (1991). Purification and developmental analysis of the major anionic peroxidases from the seed coat of Glycine max. Plant Physiol. 96, 214–220. 10.1104/pp.96.1.214 PubMed DOI PMC

Girin T., Paicu T., Stephenson P., Fuentes S., Korner E., O'Brien M., et al. . (2011). INDEHISCENT and SPATULA interactto specify carpel and valve margin tissue and thus promote seed dispersal in Arabidopsis. Plant Cell 23, 3641–3653. 10.1105/tpc.111.090944 PubMed DOI PMC

Graeber K., Nakabayashi K., Miatton E., Leubner-Metzger G., Soppe W. J. J. (2012). Molecular mechanisms of seed dormancy. Plant Cell Environ. 35, 1769–1786. 10.1111/j.1365-3040.2012.02542.x PubMed DOI

Grant W. F. (1996). Seed pod shattering in the genus Lotus (Fabaceae): a synthesis of diverse evidence. Can. J. Plant Sci. 76, 447–456. 10.4141/cjps96-079 DOI

Hammer K. (1984). Das Domestikationssyndrom. Kulturpflanze 32, 11–34. 10.1007/BF02098682 DOI

Hedley C. L., Smith C. M., Ambrose M. J., Cook S., Wang T. L. (1986). An analysis of seed development in Pisum sativum. The effect of the r-locus on the growth and development of the seed. Ann. Bot. 58, 371–379. 10.1093/oxfordjournals.aob.a087215 DOI

Hellens R. P., Moreau C., Lin-Wang K., Schwinn K. E., Thomson S. J., Fiers M. W., et al. . (2010). Identification of Mendel's white flower character. PLoS ONE 5:e13230. 10.1371/journal.pone.0013230 PubMed DOI PMC

Isemura T., Kaga A., Tabata S., Somta P., Srinives P., Shimizu T., et al. . (2012). Construction of a genetic linkage map and genetic analysis of domestication related traits in mungbean (Vigna radiata). PLoS ONE 7:e41304. 10.1371/journal.pone.0139666 PubMed DOI PMC

Jang S. J., Sato M., Sato K., Jitsuyama Y., Fujino K., Mori H., et al. . (2015). A single-nucleotide polymorphism in an endo-1,4-β-glucanase gene controls seed coat permeability in soybean. PLoS ONE 10:e0128527. 10.1371/journal.pone.0128527 PubMed DOI PMC

Kahl G., Molina C., Rotter B., Jüngling R., Frank A., Krezdorn N., et al. (2012). Reduced representation sequencing of plant stress transcriptomes. J. Plant Biochem. Biotechnol. 21, 119–127. 10.1007/s13562-012-0129-y DOI

Kalendar R., Lee D., Schulman A. H. (2014). FastPCR software for PCR, in silico PCR, and oligonucleotide assembly and analysis, in DNA Cloning and Assembly Methods, Vol. 1116, Methods in Molecular Biology, eds Valla S., Lale R. (New York, NY: Springer; ), 271–302. 10.1007/978-1-62703-764-8_18 PubMed DOI

Kantar F., Pilbeam C. J., Hebblethwaite P. D. (1996). Effect of tannin content of faba bean (Vicia faba) seed on seed vigour, germination and field emergence. Ann. Appl. Biol. 128, 85–93. 10.1111/j.1744-7348.1996.tb07092.x DOI

Kaur S., Pembleton L. W., Cogan N. O., Savin K. W., Leonforte T., Paull J., et al. . (2012). Transcriptome sequencing of field pea and faba bean for discovery and validation of SSR genetic markers. BMC Genomics 13:104. 10.1186/1471-2164-13-104 PubMed DOI PMC

Kislev M. E., Bar-Yosef O. (1988). The legumes: the earliest domesticated plants in the Near East? Curr. Anthropol. 29, 175–179. 10.1086/203623 DOI

Koinange E. M. K., Singh S., Gepts P. (1996). Genetic control of the domestication syndrome in common bean. Crop Sci. 36, 1037–1045. 10.2135/cropsci1996.0011183X003600040037x DOI

Koizumi M., Kaori K., Seiichiro I., Nobuaki I., Shighiro N., Hiromi K. (2008). Role of seed coat in imbibing soybean seed observed by micro-magnetic resonance imaging. Ann. Bot. 102, 343–352. 10.1093/aob/mcn095 PubMed DOI PMC

Kongjaimun A., Kaga A., Tomooka N., Somta P., Vaughan D. A., Srinives P. (2012). The genetics of domestication of yardlongbean, Vigna unguiculata (L.) Walp. ssp. unguiculata cv.-gr. sesquipedalis. Ann. Bot. 109, 1185–1200. 10.1093/aob/mcs048 PubMed DOI PMC

Konishi S., Izawa T., Lin S. Y., Ebana K., Fukuta Y., Sasaki T., et al. . (2006). An SNP caused loss of seed shattering during rice domestication. Science 312, 1392–1396. 10.1126/science.1126410 PubMed DOI

Korban S. S., Coyne D. P., Weihing J. L. (1981). Evaluation, variation, and genetic control of seed coat whiteness in dry beans (Phaseolus vulgaris L.). J. Am. Soc. Hortic. Sci. 166, 575–579.

Kour A., Boone A. M., Vodkin L. O. (2014). RNA-Seq profiling of a defective seed coat mutation in Glycine max reveals differential expression of proline-rich and other cell wall protein transcripts. PLoS ONE 9:e96342. 10.1371/journal.pone.0096342 PubMed DOI PMC

Krygier K., Frank Sosulski F., Hogge L. (1982). Free, esterified, and insoluble-bound phenolic acids. 1. Extraction and purification procedure. J. Agric. Food Chem. 30, 330–334. 10.1021/jf00110a028 DOI

Kučera L., Kurka O., Barták P., Bednář P. (2017). Liquid chromatography/high resolution tandem mass spectrometry - tool for the study of polyphenol profile changes during micro-scale biogas digestion of grape marcs. Chemosphere 166, 463–472. 10.1016/j.chemosphere.2016.09.124 PubMed DOI

Kujur A., Bajaj D., Upadhyaya H. D., Das S., Ranjan R., Shree T., et al. . (2015). A genome-wide SNP scan accelerates trait-regulatory genomic loci identification in chickpea. Sci. Rep. 5:11166. 10.1038/srep11166 PubMed DOI PMC

Ladizinsky G. (1998). Plant Evolution under Domestication. Dordrecht: Kluwer Academic Publishers.

Lamport D. T. A., Kieliszewski M. J., Chen Y., Cannon M. C. (2011). Role of the Extensin superfamily in primary cell wall architecture. Plant Physiol. 156, 11–19. 10.1104/pp.110.169011 PubMed DOI PMC

Legesse N., Powell A. A. (1996). Relationship between the development of seed coat pigmentation, seed coat adherence to the cotyledons and the rate of imbibition during the maturation of grain legumes. Seed Sci. Technol. 24, 23–32.

Lenser T., Theißen G. (2013). Molecular mechanisms involved in convergent crop domestication. Trends Plant Sci. 18, 704–714. 10.1016/j.tplants.2013.08.007 PubMed DOI

Lepiniec L., Debeaujon I., Routaboul J. M., Baudry A., Pourcel L., Nesi N., et al. . (2006). Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57, 405–430. 10.1146/annurev.arplant.57.032905.105252 PubMed DOI

Li P., Chen B., Zhang G., Chen L., Dong Q., Wen J., et al. . (2016b). Regulation of anthocyanin and proanthocyanidin biosynthesis by Medicago truncatula bHLH transcription factor MtTT8. New Phytol. 210, 905–921. 10.1111/nph.13816 PubMed DOI

Li P., Dong Q., Ge S., He X., Verdier J., Li D., et al. . (2016a). Metabolic engineering of proanthocyanidin production by repressing the isoflavone pathways and redirecting anthocyanidin precursor flux in legume. Plant Biotechnol. J. 14, 1604–1618. 10.1111/pbi.12524 PubMed DOI PMC

Li Y.-G., Tanner G., Larkin P. (1996). The DMACA–HCl protocol and the threshold proanthocyanidin content for bloat safety in forage legumes. J. Science Food Agric. 70, 89–101. 10.1002/(SICI)1097-0010(199601)70:1<89::AID-JSFA470>3.0.CO;2-N DOI

Liljegren S. J., Ditta G. S., Eshed Y., Savidge B., Bowman J., Yanofsky M. F. (2000). SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766–770. 10.1038/35008089 PubMed DOI

Liljegren S. J., Roeder A. H., Kempin S. A., Gremski K., Østergaard L., Guimil S., et al. . (2004). Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116, 843–853. 10.1016/S0092-8674(04)00217-X PubMed DOI

Liu C., Jun J. H., Dixon R. A. (2014). MYB5 and MYB14 play pivotal roles in seed coat polymer biosynthesis in Medicago truncatula. Plant Physiol. 165, 1424–1439. 10.1104/pp.114.241877 PubMed DOI PMC

Liu N., Zhang G., Xu S., Mao W., Hu Q., Gong Y. (2015). Comparative transcriptomic analyses of vegetable and grain pea (Pisum sativum L.) seed development. Front. Plant Sci. 6:1039. 10.3389/fpls.2015.01039 PubMed DOI PMC

Lopez-Amoros M. L., Hernandez T., Estrella I. (2006). Effect of germination on legume phenolic compounds and their antioxidant activity. J. Food Compost. Anal. 19, 277–283. 10.1016/j.jfca.2004.06.012 DOI

Ma F., Cholewa E., Mohamed T., Peterson C. A., Gijzen M. (2004). Cracks in the palisade cuticle of soybean seed coats correlate with their permeability to water. Ann. Bot. 94, 213–228. 10.1093/aob/mch133 PubMed DOI PMC

Marbach I., Mayer A. M. (1974). Permeability of seed coats to water as related to drying conditions and metabolism of phenolics. Plant Physiol. 54, 817–820. 10.1104/pp.54.6.817 PubMed DOI PMC

Marles M. A. S., Vandenberg A., Bett K. E. (2008). Polyphenol oxidase activity and differential accumulation of polyphenolics in seed coats of pinto bean (Phaseolus vulgaris L.) characterize postharvest color changes. J. Agric. Food Chem. 56, 7049–7056. 10.1021/jf8004367 PubMed DOI

Matus A., Slinkard A. E. (1993). Effect of fungicidal seed treatment on zero-tannin lentil. Lens Newsl. 20, 46–50.

McCarty D. R. (1986). A simple method for extraction of DNA from maize tissue. Maize Genet. Coop. Newsl. 60, 61.

McDonald M. B., Vertucci C. W., Roos E. E. (1988). Soybean seed imbibition: water absorption by seed parts. Crop Sci. 28, 993–997. 10.2135/cropsci1988.0011183X002800060026x DOI

Meyer C. J., Steudle E., Peterson C. A. (2007). Patterns and kinetics of water uptake by soybean seeds. J. Exp. Bot. 58, 717–732. 10.1093/jxb/erl244 PubMed DOI

Meyer R. S., Purugganan M. D. (2013). Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840–852. 10.1038/nrg3605 PubMed DOI

Meyer R. S., DuVal A. E., Jensen H. R. (2012). Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytol. 196, 29–48. 10.1111/j.1469-8137.2012.04253.x PubMed DOI

Miao Z. H., Fortune J. A., Gallagher J. (2001). Anatomical structure and nutritive value of lupin seed coats. Aust. J. Agric. Res. 52, 985–993. 10.1071/AR00117 DOI

Michelmore R. W., Paran I., Kesseli R. V. (1991). Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. U.S.A. 88, 9828–9832. 10.1073/pnas.88.21.9828 PubMed DOI PMC

Mitsuda N., Ohme-Takagi M. (2008). NAC transcription factors NST1 and NST3 regulate pod shattering in a partially redundant manner by promoting secondary wall formation after the establishment of tissue identity. Plant J. 56, 768–778. 10.1111/j.1365-313X.2008.03633.x PubMed DOI

Moïse J. A., Han S., Gudynaite-Savitch L., Johnson D. A., Miki B. L. A. (2005). Seed coats: structure, development, composition, and biotechnology. In vitro Cell. Dev. Biol. Plant 41, 620–644. 10.1079/IVP2005686 DOI

Moreau C., Mike J., Ambrose M. J., Turner L., Hill L., Ellis T. H. N., et al. . (2012). The b gene of pea encodes a defective flavonoid 3′,5′-hydroxylase, and confers pink flower color. Plant Physiol. 159, 759–768. 10.1104/pp.112.197517 PubMed DOI PMC

Mullin W. J., Xu W. (2000). A study of the intervarietal differences of cotyledon and seed coat carbohydrates in soybean. Food Res. Int. 33, 883–891. 10.1016/S0963-9969(00)00118-6 DOI

Mullin W. J., Xu W. (2001). Study of soybean seed coat components and their relationship to water absorption. J. Agric. Food Chem. 49, 5331–5335. 10.1021/jf010303s PubMed DOI

Nikolaeva M. G. (1969). Physiology of Deep Dormancy in Seeds. Leningrad, Russia, Izdatelstvo ‘Nauka’. Transl. by Shapiroin Russian Z. Washington, DC: National Science Foundation.

Nonogaki H. (2014). Seed dormancy and germination – emerging mechanisms and new hypotheses. Front. Plant Sci. 5:233. 10.3389/fpls.2014.00233 PubMed DOI PMC

North N., Casey R., Domoney C. (1989). Inheritance and mapping of seed lipoxygenase polypeptides in Pisum. Theor. Appl. Genet. 77, 805–808. 10.1007/BF00268330 PubMed DOI

Olsen K. M., Wendel J. F. (2013). A bountiful harvest: genomic insights into crop domestication phenotypes. Annu. Rev. Plant Biol. 64, 47–70. 10.1146/annurev-arplant-050312-120048 PubMed DOI

Patil G., Valliyodan B., Deshmukh R., Prince S., Nicander B., Zhao M., et al. (2015). Soybean (Glycin max) SWEET gene family: insight through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genomics 16:520 10.1186/s12864-015-1730-y PubMed DOI PMC

Pazhamala L. T., Agarwal G., Bajaj P., Kumar V., Kulshreshtha A., Saxena R. K., et al. . (2016). Deciphering transcriptional programming during pod and seed development using RNA-Seq in pigeonpea (Cajanus cajan). PLoS ONE 11:e0164959. 10.1371/journal.pone.0164959 PubMed DOI PMC

Pizzi A., Cameron F. A. (1986). Flavonoid tannins — structural wood components for drought-resistance mechanisms of plants. Wood Sci. Technol. 20:119.

Porter L. J. (1989). Condensed tannins, in Natural Products of Woody Plants I: Chemicals Extraneous to the Lignocellulosic Cell, ed Rowe J. W. (Berlin: Springer; ), 651–690. 10.1007/978-3-642-74075-6_18 DOI

Pradhan S., Bandhiwal N., Shah N., Kant C., Gaur R., Bhatia S. (2014). Global transctriptome analysis of developing chickpea (Cicer arietinum L.) seeds. Front. Plant Sci. 5:698. 10.3389/fpls.2014.00698 PubMed DOI PMC

Purugganan M. D., Fuller D. Q. (2009). The nature of selection during plant domestication. Nature 457, 843–848. 10.1038/nature07895 PubMed DOI

Radchuk V., Borisjuk L. (2014). Physical, metabolic and developmental functions of the seed coat. Front. Plant Sci. 5:510. 10.3389/fpls.2014.00510 PubMed DOI PMC

Ramsay G. (1997). Inheritance and linkage of a gene for testa imposed seed dormancy in faba bean (Vicia faba L.). Plant Breed. 116, 287–289. 10.1111/j.1439-0523.1997.tb00998.x DOI

Ranal M. A., Santana D. G. (2006). How and why to measure the germination process? Rev. Bras. Bot. 29, 1–11. 10.1590/S0100-84042006000100002 DOI

Ranathunge K., Shao S., Qutob D., Gijzen M., Peterson C. A., Bernards M. A. (2010). Properties of the soybean seed coat cuticle change during development. Planta 231, 1171–1188. 10.1007/s00425-010-1118-9 PubMed DOI

Redekar N. R., Biyashev R. M., Jensen R. V., Helm R. F., Grabau E. A., Maroof M. A. (2015). Genome-wide transcriptome analyses of developing seeds from low and normal phytic acid soybean lines. BMC Genomics 16:1074. 10.1186/s12864-015-2283-9 PubMed DOI PMC

Righetti K., Vu J. L., Pelletier S., Vu B. L., Glaab E., Lalanne D., et al. . (2015). Inference of longevity-related genes from a robust coexpression network of seed maturation identifies regulators linking seed storability to biotic defense-related pathways. Plant Cell 27, 2692–2708. 10.1105/tpc.15.00632 PubMed DOI PMC

Robert C., Watson M. (2015). Errors in RNA-Seq quantification affect genes of relevance to human disease. Genome Biol. 16:177. 10.1186/s13059-015-0734-x PubMed DOI PMC

Roth A., Ding J., Morin R., Crisan A., Ha G., Giuliany R., et al. . (2012). JointSNVMix: a probabilistic model for accurate detection of somatic mutations in normal/tumour paired next-generation sequencing data. Bioinformatics 28, 907–913. 10.1093/bioinformatics/bts053 PubMed DOI PMC

Schmutz J., McClean P. E., Mamidi S., Wu G. A., Cannon S. B., Grimwood J., et al. . (2014). A reference genome for common bean and genome-wide analysis of dual domestications. Nat. Genet. 46, 707–713. 10.1038/ng.3008 PubMed DOI PMC

Seiki M. (1999). Membrane-type matrix metalloproteinases. Acta Pathol. Microbiol. Immunol. Scand. 107, 137–143. PubMed

Severin A., Woody J. L., Bolon Y.-T., Joseph B., Diers B. W., Farmer A. D., et al. . (2010). RNA-Seq atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10:160. 10.1186/1471-2229-10-160 PubMed DOI PMC

Shao S., Meyer C. J., Ma F., Peterson C. A., Bernards M. A. (2007). The outermost cuticle of soybean seeds: chemical composition and function during imbibition. J. Exp. Bot. 58, 1071–1082. 10.1093/jxb/erl268 PubMed DOI

Shi J., Lai J. (2015). Patterns of genomic changes with crop domestication and breeding. Curr. Opin. Plant Biol. 24, 47–53. 10.1016/j.pbi.2015.01.008 PubMed DOI

Singh R., Singh S., Parihar P., Mishra R. K., Tripathi D. K., Singh V. P., et al. (2016). Reactive oxygen species (ROS): beneficial companions of plant's developmental processes. Front. Plant Sci. 7:1299 10.3389/fpls.2016.01299 PubMed DOI PMC

Smartt J. (1990). Grain Legumes: Evolution and Genetic Resources. Cambridge, UK: Cambridge University Press; 10.1017/cbo9780511525483 DOI

Smýkal P., Aubert G., Burstin J., Coyne C. J., Ellis N. T. H., Flavell A. J., et al. (2012). Pea (Pisum sativum L.) in the genomic era. Agronomy 2, 74–115. 10.3390/agronomy2020074 DOI

Smýkal P., Coyne C. J., Ambrose M. J., Maxted N., Schaefer H., Blair M. W., et al. (2015). Legume crops phylogeny and genetic diversity for science and breeding. Crit. Rev. Plant Sci. 34, 43–104. 10.1080/07352689.2014.897904 DOI

Smýkal P., Vernoud V., Blair M. W., Soukup A., Thompson R. D. (2014). The role of the testa during development and in establishment of dormancy of the legume seed. Front. Plant Sci. 5:351. 10.3389/fpls.2014.00351 PubMed DOI PMC

Soukup A. (2014). Selected simple methods of plant cell wall histochemistry and staining for light microscopy, in Plant Cell Morphogenesis: Methods and Protocols, Vol. 1080, Methods in Molecular Biology, eds Žársky V., Cvrčková F. (New York, NY: Springer; ), 25–40. 10.1007/978-1-62703-643-6_2 PubMed DOI

Soukup A., Tylová E. (2014). Essential methods of plant sample preparation for light microscopy, in Plant Cell Morphogenesis: Methods and Protocols, Vol. 1080, Methods in Molecular Biology, eds Žársky V., Cvrčková F. (New York, NY: Springer; ), 1–23. 10.1007/978-1-62703-643-6_1 PubMed DOI

Sreerama N. Y., Sashikala V. B., Pratape V. M. (2010). Variability in the distribution of phenolic compounds in milled fractions of chickpea and horse gram: evaluation of their antioxidant properties. J. Agric. Food Chem. 58, 8322–8330. 10.1021/jf101335r PubMed DOI

Suanum W., Somta P., Kongjaimun A., Yimram T., Kage A., Tomooka N., et al. (2016). Co-localization of QTLs for pod fiber content and pod shattering in F-2 and backcross populations between yardlong bean and wild cowpea. Mol. Breeding 36, 80 10.1007/s11032-016-0505-8 DOI

Sudheesh J., Sawbridge T. I., Cogan N. O., Kennedy P., Forster J. W., Kaur S. (2015). De novo assembly and characterization of field pea transcriptome using RNA-Seq. BMC Genomics 16:611 10.1186/s12864-015-1815-7 PubMed DOI PMC

Sun L., Miao Z., Cai C., Zhang D., Zhao M., Wu Y., et al. . (2015). GmHs1-1, encoding a calcineurin-like protein, controls hard-seededness in soybean. Nat. Genet. 47, 939–943. 10.1038/ng.3339 PubMed DOI

Suzuki M., Fujino K., Nakamoto Y., Ishimoto M., Funatsuki H. (2010). Fine mapping and development of DNA markers for the qPDH1 locus associated with pod dehiscence in soybean. Mol. Breed. 25, 407–418. 10.1007/s11032-009-9340-5 DOI

Tayeh N., Aluome C., Falque M., Jacquin F., Klein A., Chauveau A., et al. . (2015). Development of two major resources for pea genomics: the GenoPea 13.2K SNP Array and a high density, high resolution consensus genetic map. Plant J. 84, 1257–1273. 10.1111/tpj.13070 PubMed DOI

Tiwari S. P., Bhatia V. S. (1995). Characters of pod anatomy associated with resistance to pod-shattering in soybean. Ann. Bot. 76, 483–485. 10.1006/anbo.1995.1123 DOI

Troszyńska A., Ciska E. (2002). Phenolic compounds of seed coats of white and coloured varieties of pea (Pisum sativum L.) and their total antioxidant activity. Czech J. Food Sci. 20, 15–22.

Trygg J., Wold S. (2002). Orthogonal projections to latent structures (O-PLS). J. Chemometrics 16, 119–128. 10.1002/cem.695 DOI

Tuteja J. H., Clough S. J., Chan W. C., Vodkin L. O. (2004). Tissue specific gene silencing mediated by anaturally occurring chalcone synthase gene cluster in Glycine max. Plant Cell 16, 819–835. 10.1105/tpc.021352 PubMed DOI PMC

Verdier J., Dessaint F., Schneider C., Abirached-Darmency M. (2013a). A combined histology and transcriptome analysis unravels novel questions on Medicago truncatula seed coat. J. Exp. Bot. 64, 459–470. 10.1093/jxb/ers304 PubMed DOI PMC

Verdier J., Torres-Jerez I., Wang M., Andriankaja A., Allen S. N., He J., et al. . (2013b). Establishment of the Lotus japonicus gene expression atlas (LjGEA) and its use to explore legume seed maturation. Plant J. 74, 351–362. 10.1111/tpj.12119 PubMed DOI

Vu D. T., Velusamy V., Park E. (2014). Structure and chemical composition of wild soybean seed coat related to its permeability. Pak. J. Bot. 46, 1847–1857.

Wan L., Li B., Pandey M. K., Wu Y., Lei Y., Yan L., et al. . (2016). Transcriptome analysis of a new peanut seed coat mutant for the physiological regulatory mechanism involved in seed coat cracking and pigmentation. Front. Plant Sci. 7:1491. 10.3389/fpls.2016.01491 PubMed DOI PMC

Wang C. S., Vodkin L. O. (1994). Extraction of RNA from tissues containing high levels of proanthocyanidins that bind RNA. Plant Mol. Biol. Rep. 12, 132–145.

Wang H. L., Grusak M. A. (2005). Structure and development of Medicago truncatula pod wall and seed coat. Ann. Bot. 95, 737–747. 10.1093/aob/mci080 PubMed DOI PMC

Wang L., Feng Z., Wang X., Wang X., Zhang X. (2010). DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136–138. 10.1093/bioinformatics/btp612 PubMed DOI

Weeden N. F. (2007). Genetic changes accompanynig the domestication of Pisum sativum: is there a common genetic basis to the Domestication syndrome for legumes? Ann. Bot. 100, 1017–1025. 10.1093/aob/mcm122 PubMed DOI PMC

Weeden N. F., Brauner S., Przyborowski J. A. (2002). Genetic analysis of pod dehistance in pea (Pisum sativum L.). Cell. Mol. Biol. Lett. 7, 657–663. PubMed

Weitbrecht K., Muller K., Leubner-Metzger G. (2011). First off the mark: early seed germination. J. Exp. Bot. 62, 3289–3309. 10.1093/jxb/err030 PubMed DOI

Werker E., Marbach I., Mayer A. M. (1979). Relation between the anatomy of the testa, water permeability and the presence of phenolics in the genus Pisum. Ann. Bot. 43, 765–771. 10.1093/oxfordjournals.aob.a085691 DOI

Xie D. Y., Sharma S. B., Dixon R. A. (2004). Anthocyanidin reductases from Medicago truncatula and Arabidopsis thaliana. Arch. Biochem. Biophys. 422, 91–102. 10.1016/j.abb.2003.12.011 PubMed DOI

Xie D. Y., Sharma S. B., Paiva N. L., Ferreira D., Dixon R. A. (2003). Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299, 396–399. 10.1126/science.1078540 PubMed DOI

Yang K., Jeong N., Moon J., Lee Y. H., Lee S. H., Kim H. M., et al. . (2010). Genetic analysis of genes controlling natural variation of seed coat and flower colors in soybean. J. Heredity 101, 757–768. 10.1093/jhered/esq078 PubMed DOI

Yin Q., Shen G., Chang Z., Tang Y., Gao H., Pang Y. (2017). Involvement of three putative glucosyltransferases from the UGT72 family in flavonol glucoside/rhamnoside biosynthesis in Lotus japonicus seeds. J. Exp. Bot. 68, 597–612. 10.1093/jxb/erw420 PubMed DOI PMC

Young M. D., Wakefield M. J., Smyth G. K., Oshlack A. (2010). Gene ontology analysis for RNA-Seq: accounting for selection bias. Genome Biol. 11:R14. 10.1186/gb-2010-11-2-r14 PubMed DOI PMC

Zawada A. M., Rogacev K., Müller S., Rotter B., Winter P., Fliser D., et al. . (2014). Massive analysis of cDNA ends (MACE) and miRNA expression profiling identifies proatherogenic pathways in chronic kidney disease. Epigenetics 9, 161–172. 10.4161/epi.26931 PubMed DOI PMC

Zhang S., Shi Y., Cheng N., Du H., Fan W., Wang C. (2015). De novo characterization of fall dormant and nondormant alfalfa (Medicago sativa L.) leaf transcriptome and identification of candidate genes related to fall dormancy. PLoS ONE 10:e0122170. 10.1371/journal.pone.0122170 PubMed DOI PMC

Zhao J., Pang Y., Dixon R. A. (2010). The mysteries of proanthocyanidin transport and polymerization. Plant Physiol. 153, 437–443. 10.1104/pp.110.155432 PubMed DOI PMC

Zhao Q., Dixon R. A. (2011). Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci. 16, 227–233. 10.1016/j.tplants.2010.12.005 PubMed DOI

Zhao S., Tuan P. A., Li X., Kim Y. B., Kim H., Park C. G., et al. . (2013). Identification of phenylpropanoid biosynthetic genes and phenylpropanoid accumulation by transcriptome analysis of Lycium chinense. BMC Genomics 14:802. 10.1186/1471-2164-14-802 PubMed DOI PMC

Zhong R., Lee C., Ye Z. (2010). Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trend Plant Sci. 15, 625–632. 10.1016/j.tplants.2010.08.007 PubMed DOI

Zhou S., Sekizuka H., Yang Z., Sawa S., Pan J. (2010). Phenolics in the seed coat of wild soybean (Glycine soja) and their significance for seed hardness and seed germination. J. Agric. Food Chem. 58, 10972–10978. 10.1021/jf102694k PubMed DOI

Zhou Z., Jiang Y., Wang Z., Gou Z., Lyu J., Li W., et al. . (2015). Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nature Biotech. 33, 408–414. 10.1038/nbt.3096 PubMed DOI

Zhu W., Chen X., Li H., Zhu F., Hong Y., Varshney R. K., et al. . (2014). Comparative transcriptome analysis of aerial and subterranean pods development provides insights into seed abortion in peanut. Plant Mol. Biol. 85, 395–409. 10.1007/s11103-014-0193-x PubMed DOI PMC

Zhukov V. A., Zhernakov A. I., Kulaeva O. A., Ershov N. I., Borisov A. Y., Tikhonovich I. A. (2015). De novo assembly of the Pea (Pisum sativum L.) nodule transcriptome. Int. J. Genomics 2015:695947. 10.1155/2015/695947 PubMed DOI PMC

Zohary D., Hopf M. (2000). Domestication of Plants in the Old World, 3rd Edn. New York, NY: Oxford University Press.

Zou H., Tzarfati R., Hübner S., Krugman T., Fahima T., Abbo S., et al. . (2015). Transcriptome profiling of wheat glumes in wild emmer, hulled landraces and modern cultivars. BMC Genomics 16:777. 10.1186/s12864-015-1996-0 PubMed DOI PMC

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