Paralogous Gene Recruitment in Multiple Families Constitutes Genetic Architecture and Robustness of Pod Dehiscence in Legumes
Language English Country Great Britain, England Media print
Document type Journal Article
Grant support
31930007
National Natural Science Foundation of China
19-07155S
Grant Agency of the Czech Republic
PrF-2023-001
Palacky University Grant Agency
PubMed
39657612
PubMed Central
PMC11652722
DOI
10.1093/gbe/evae267
PII: 7918796
Knihovny.cz E-resources
- Keywords
- domestication, gene expression, genetic basis, legumes, lignin, pod dehiscence,
- MeSH
- Cell Wall metabolism genetics MeSH
- Fabaceae * genetics MeSH
- Lignin metabolism MeSH
- Multigene Family MeSH
- Gene Expression Regulation, Plant MeSH
- Plant Proteins genetics MeSH
- Seeds genetics MeSH
- Transcriptome MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Lignin MeSH
- Plant Proteins MeSH
Pod dehiscence facilitates seed dispersal in wild legumes while indehiscence is a key domestication trait in cultivated ones. However, the evolutionary genetic mechanisms underlying its diversity are largely unclear. In this study, we compared transcriptomes of two warm-season (Glycine spp. and Phaseolus spp.) and two cool-season (Pisum spp. and Medicago ruthenica) legumes in analysis of dehiscent and indehiscent pod genotypes. Differentially expressed genes in AP2/ERF-like transcription factors and seven structural gene families, including lactoperoxidase, laccase, and cellulose synthase-interactive proteins, which are involved in secondary cell wall component accumulation, were identified to exert key roles in pod dehiscence variation. In accordance with this, higher lignin and cellulose contents were observed in pod secondary cell wall of dehiscent accessions of soybean and pea; however, the variation patterns of lignin polymers in soybean (accumulation) and pea (proportion) differed between dehiscent and indehiscent pods. Moreover, genome-wide comparative analysis revealed that orthogroups represented <1% of all identified differentially expressed genes could be traced among the four genera of legumes, while recruiting paralogous members may constitute the genetic robustness of legume pod dehiscence. This study compared the genetic mechanism among several legumes in pod dehiscence formation and revealed a compensating role of paralogous redundancy of involved gene families in seed dispersal, which can guide crop breeding.
China National Botanical Garden Beijing 100093 China
Department of Botany Faculty of Sciences Palacky University Olomouc 773 71 Czech Republic
Instituto de Recursos Naturales y Agrobiología de Sevilla CSIC 41012 Seville Spain
The Innovative Academy of Seed Design Chinese Academy of Sciences Beijing 100101 China
University of Chinese Academy of Sciences Beijing 100049 China
See more in PubMed
Aguilar-Benitez D, Rubio J, Millán T, Gil J, Die JV, Castro P. Genetic analysis reveals PDH1 as a candidate gene for control of pod dehiscence in chickpea. Mol Breeding. 2020:40(4):40. 10.1007/s11032-020-01117-9. DOI
Akazome Y, Kanda S, Okubo K, Oka Y. Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain. J Fish Biol. 2010:76(1):161–182. 10.1111/j.1095-8649.2009.02496.x. PubMed DOI
Ali S, Kucek LK, Riday H, Krom N, Krogman S, Cooper K, Jacobs L, Mehta P, Trammell M, Bhamidimarri S, et al. Transcript profiling of hairy vetch (Vicia villosa Roth) identified interesting genes for seed dormancy. Plant Genome. 2023:16(2):e20330. 10.1002/tpg2.20330. PubMed DOI
Armon S, Efrati E, Kupferman R, Sharon E. Geometry and mechanics in the opening of chiral seed pods. Science. 2011:333(6050):1726–1730. 10.1126/science.1203874. PubMed DOI
Aslan C, Beckman NG, Rogers HS, Bronstein J, Zurell D, Hartig F, Shea K, Pejchar L, Neubert M, Poulsen J, et al. Employing plant functional groups to advance seed dispersal ecology and conservation. AoB Plants. 2019:11(2):plz006. 10.1093/aobpla/plz006. PubMed DOI PMC
Azani N, Babineau M, Bailey CD, Banks H, Barbosa AR, Pinto RB, Boatwright JS, Borges LM, Brown GK, Bruneau A, et al. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: the legume phylogeny working group (LPWG). Taxon. 2017:66(1):44–77. 10.12705/661.3. DOI
Bailon-Zambrano R, Sucharov J, Mumme-Monheit A, Murry M, Stenzel A, Pulvino AT, Mitchell JM, Colborn KL, Nichols JT. Variable paralog expression underlies phenotype variation. eLife. 2022:11:e79247. 10.7554/eLife.79247. PubMed DOI PMC
Balarynová J, Klčová B, Sekaninová J, Kobrlová L, Cechová MZ, Krejčí P, Leonova T, Gorbach D, Ihling C, Smržová L, et al. The loss of polyphenol oxidase function is associated with hilum pigmentation and has been selected during pea domestication. New Phytol. 2022:235(5):1807–1821. 10.1111/nph.18256. PubMed DOI
Ballester P, Ferrándiz C. Shattering fruits: variations on a dehiscent theme. Curr Opin Plant Biol. 2017:35:68–75. 10.1016/j.pbi.2016.11.008. PubMed DOI
Boerjan W, Ralph J, Baucher M. Lignin biosynthesis. Annu Rev Plant Biol. 2003:54(1):519–546. 10.1146/annurev.arplant.54.031902.134938. PubMed DOI
Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol. 2021:38(12):5825–5829. 10.1093/molbev/msab293. PubMed DOI PMC
Cao H, Chen J, Yue M, Xu C, Jian W, Liu Y, Song B, Gao Y, Cheng Y, Li Z. Tomato transcriptional repressor MYB70 directly regulates ethylene-dependent fruit ripening. Plant J. 2020:104(6):1568–1581. 10.1111/tpj.15021. PubMed DOI
Cao M-J, Zhang Y-L, Liu X, Huang H, Zhou XE, Wang W-L, Zeng A, Zhao C-Z, Si T, Du J, et al. Combining chemical and genetic approaches to increase drought resistance in plants. Nat Commun. 2017:30(1):1183. 10.1038/s41467-017-01239-3. PubMed DOI PMC
Cao Z, Socquet-Juglard D, Daba K, Vandenberg A, Bett KE. Understanding genome structure facilitates the use of wild lentil germplasm for breeding: a case study with shattering loci. Plant Genome. 2024:17(2):e20455. 10.1002/tpg2.20455. PubMed DOI
Cárdenas PD, Almeida A, Bak S. Evolution of structural diversity of triterpenoids. Front Plant Sci. 2019:10:1523. 10.3389/fpls.2019.01523. PubMed DOI PMC
Chamberlain-Irwin HN, Hufford MB. Convergent domestication: finding the genes that make crops. Curr Biol. 2022:32(12):R585–R588. 10.1016/j.cub.2022.05.003. PubMed DOI
Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018:34(17):884–890. 10.1093/bioinformatics/bty560. PubMed DOI PMC
Dai Y, Luo L, Zhao Z. Genetic robustness control of auxin output in priming organ initiation. Proc Natl Acad Sci U S A. 2023:120(28):e2221606120. 10.1073/pnas.2221606120. PubMed DOI PMC
Diss G, Ascencio D, DeLuna A, Landry CR. Molecular mechanisms of paralogous compensation and the robustness of cellular networks. J Exp Zool B Mol Dev Evol. 2014:322(7):488–499. 10.1002/jez.b.22555. PubMed DOI
Di Vittori V, Bitocchi E, Rodriguez M, Alseekh S, Bellucci E, Nanni L, Gioia T, Marzario S, Logozzo G, Rossato M, et al. Pod indehiscence in common bean is associated with the fine regulation of PvMYB26. J Exp Bot. 2021:72(5):1617–1633. 10.1093/jxb/eraa553. PubMed DOI PMC
Di Vittori V, Gioia T, Rodriguez M, Bellucci E, Bitocchi E, Nanni L, Attene G, Rau D, Papa R. Convergent evolution of the seed shattering trait. Genes (Basel). 2019:10(1):68. 10.3390/genes10010068. PubMed DOI PMC
Dong XM, Chen JW, Zhou Q, Luo D, Fang LF, Liu WX, Liu ZP. Pod-shattering characteristic differences between shattering-resistant and shattering-susceptible common vetch accessions are associated with lignin biosynthesis. J Integr Agr. 10.1016/j.jia.2024.03.032, 2024, preprint: not peer reviewed. DOI
Dong Y, Yang X, Liu J, Wang B-H, Liu B-L, Wang Y-Z. Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean. Nat Commun. 2014:5(1):3352. 10.1038/ncomms4352. PubMed DOI
Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004:5(1):113. 10.1186/1471-2105-5-113. PubMed DOI PMC
Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Bio. 2019:20(1):238. 10.1186/s13059-019-1832-y. PubMed DOI PMC
Félix M-A, Wagner A. Robustness and evolution: concepts, insights and challenges from a developmental model system. Heredity (Edinb). 2008:100(2):132–140. 10.1038/sj.hdy.6800915. PubMed DOI
Forlani S, Masiero S, Mizzotti C. Fruit ripening: the role of hormones, cell wall modifications, and their relationship with pathogens. J Exp Bot. 2019:70(11):2993–3006. 10.1093/jxb/erz112. PubMed DOI
Forlani S, Mizzotti C, Masiero S. The NAC side of the fruit: tuning of fruit development and maturation. BMC Plant Biol. 2021:21(1):238. 10.1186/s12870-021-03029-y. PubMed DOI PMC
Fourquin C, del Cerro C, Victoria FC, Vialette-Guiraud A, de Oliveira AC, Ferrándiz C. A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in Medicago genus. Plant Physiol. 2013:162(2):907–917. 10.1104/pp.113.217570. PubMed DOI PMC
Fu C, Chen H, Gao H, Lu Y, Han C, Han Y. Two papaya MYB proteins function in fruit ripening by regulating some genes involved in cell-wall degradation and carotenoid biosynthesis. J Sci Food Agric. 2020:100(12):4442–4448. 10.1002/jsfa.10484. PubMed DOI
Fuller DQ, Allaby R. Seed dispersal and crop domestication: shattering, germination and seasonality in evolution under cultivation. In: Østergaard L, editor. Annual plant reviews volume 38: fruit development and seed dispersal. Oxford: Wiley-Blackwell; 2009. p. 238–295. 10.1002/9781444314557.ch7. DOI
Fuller DQ, Denham T, Arroyo-Kalin M, Lucas L, Stevens CJ, Qin L, Allaby RG, Purugganan MD. Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record. Proc Natl Acad Sci U S A. 2014:111(17):6147–6152. 10.1073/pnas.1308937110. PubMed DOI PMC
Funatsuki H, Suzuki M, Hirose A, Inaba H, Yamada T, Hajika M, Komatsu K, Katayama T, Sayama T, Ishimoto M, et al. Molecular basis of a shattering resistance boosting global dissemination of soybean. Proc Natl Acad Sci U S A. 2014:111(50):17797–17802. 10.1073/pnas.1417282111. PubMed DOI PMC
Gu C, Guo Z-H, Hao P-P, Wang G-M, Jin Z-M, Zhang S-L. Multiple regulatory roles of AP2/ERF transcription factor in angiosperm. Bot Stud. 2017:58(1):6. 10.1186/s40529-016-0159-1. PubMed DOI PMC
Guo MW, Zhu L, Li HY, Liu WP, Wu ZN, Wang CH, Liu L, Li ZY, Li J. Mechanism of pod shattering in the forage legume Medicago ruthenica. Plant Physiol Biochem. 2022:185:260–267. 10.1016/j.plaphy.2022.06.013. PubMed DOI
Hammer K. Das Domestikationssyndrom. Kulturpflanze. 1984:32(1):11–34. 10.1007/BF02098682. DOI
Han J, Han D, Guo Y, Yan H, Wei Z, Tian Y, Qiu L. QTL mapping pod dehiscence resistance in soybean (Glycine max L. Merr.) using specific-locus amplified fragment sequencing. Theor Appl Genet. 2019:132(8):2253–2272. 10.1007/s00122-019-03352-x. PubMed DOI PMC
Hofhuis H, Moulton D, Lessinnes T, Routier-Kierzkowska A-L, Bomphrey RJ, Mosca G, Reinhardt H, Sarchet P, Gan X, Tsiantis M, et al. Morphomechanical innovation drives explosive seed dispersal. Cell. 2016:166(1):222–233. 10.1016/j.cell.2016.05.002. PubMed DOI PMC
Hradilová I, Trněný O, Válková M, Cechová M, Janská A, Prokešová L, Aamir K, Krezdorn N, Rotter B, Winter P, et al. A combined comparative transcriptomic, metabolomic, and anatomical analyses of two key domestication traits: pod dehiscence and seed dormancy in pea (Pisum sp.). Front Plant Sci. 2017:8:542. 10.3389/fpls.2017.00542. PubMed DOI PMC
Hu D, Kan G, Hu W, Li Y, Hao D, Li X, Yang H, Yang Z, He X, Huang F, et al. Identification of loci and candidate genes responsible for pod dehiscence in soybean via genome-wide association analysis across multiple environments. Front Plant Sci. 2019:10:811. 10.3389/fpls.2019.00811. PubMed DOI PMC
Iohannes SD, Jackson D. Tackling redundancy: genetic mechanisms underlying paralog compensation in plants. New Phytol. 2023:240(4):1381–1389. 10.1111/nph.19267. PubMed DOI
Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, Gao G. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 2017:45(D1):1040–1045. 10.1093/nar/gkw982. PubMed DOI PMC
Johnson LS, Eddy SR, Portugaly E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics. 2010:11(1):431. 10.1186/1471-2105-11-431. PubMed DOI PMC
Kang X, Cai J, Chen Y, Yan Y, Yang S, He R, Wang D, Zhu Y. Pod-shattering characteristics differences between two groups of soybeans are associated with specific changes in gene expression. Funct Integr Genomics. 2020:20(2):201–210. 10.1007/s10142-019-00702-2. PubMed DOI
Kessler A, Kalske A. Plant secondary metabolite diversity and species interactions. Annu Rev Ecol Evol Syst. 2018:49(1):115–138. 10.1146/annurev-ecolsys-110617-062406. DOI
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019:37(8):907–915. 10.1038/s41587-019-0201-4. PubMed DOI PMC
Koonin EV. Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet. 2005:39(1):309–338. 10.1146/annurev.genet.39.073003.114725. PubMed DOI
Kumar M, Campbell L, Turner S. Secondary cell walls: biosynthesis and manipulation. J Exp Bot. 2016:67(2):515–531. 10.1093/jxb/erv533. PubMed DOI
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008:9(1):559. 10.1186/1471-2105-9-559. PubMed DOI PMC
Lee JS, Kim KR, Ha B-K, Kang S. Identification of SNPs tightly linked to the QTL for pod shattering in soybean. Mol Breed. 2017:37(4):54. 10.1007/s11032-017-0656-2. DOI
Lenser T, Theißen G. Molecular mechanisms involved in convergent crop domestication. Trends Plant Sci. 2013:18(12):704–714. 10.1016/j.tplants.2013.08.007. PubMed DOI
Li T, Liu Z, Lv T, Xu Y, Wei Y, Liu W, Wei Y, Liu L, Wang A. Phosphorylation of MdCYTOKININ RESPONSE FACTOR4 suppresses ethylene biosynthesis during apple fruit ripening. Plant Physiol. 2023:191(1):694–714. 10.1093/plphys/kiac498. PubMed DOI PMC
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014:30(7):923–930. 10.1093/bioinformatics/btt656. PubMed DOI
Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature. 2000:404(6779):766–770. 10.1038/35008089. PubMed DOI
Liljegren SJ, Roeder AH, Kempin SA, Gremski K, Østergaard L, Guimil S, Reyes DK, Yanofsky MF. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell. 2004:116(6):843–853. 10.1016/S0092-8674(04)00217-X. PubMed DOI
Liu C, Ma T, Yuan D, Zhou Y, Long Y, Li Z, Dong Z, Duan M, Yu D, Jing Y, et al. The OsEIL1-OsERF115-target gene regulatory module controls grain size and weight in rice. Plant Biotechnol J. 2022:20(8):1470–1486. 10.1111/pbi.13825. PubMed DOI PMC
Lo S, Muñoz-Amatriaín M, Boukar O, Herniter I, Cisse N, Guo Y-N, Roberts PA, Xu S, Fatokun C, Close TJ. Identification of QTL controlling domestication-related traits in cowpea (Vigna unguiculata L. Walp). Sci Rep. 2018:8(1):6261. 10.1038/s41598-018-24349-4. PubMed DOI PMC
Lyu X, Li Y-H, Li Y, Li D, Han C, Hong H, Tian Y, Han L, Liu B, Qiu L-J. The domestication-associated L1 gene encodes a eucomic acid synthase pleiotropically modulating pod pigmentation and shattering in soybean. Mol Plant. 2023:16(7):1178–1191. 10.1016/j.molp.2023.06.003. PubMed DOI
Maity A, Lamichaney A, Joshi DC, Bajwa A, Subramanian N, Walsh M, Bagavathiannan M. Seed shattering: a trait of evolutionary importance in plants. Front Plant Sci. 2021:12:657773. 10.3389/fpls.2021.657773. PubMed DOI PMC
Marsh JI, Nestor BJ, Petereit J, Tay Fernandez CG, Bayer PE, Batley J, Edwards D. Legume-wide comparative analysis of pod shatter locus PDH1 reveals phaseoloid specificity, high cowpea expression, and stress responsive genomic context. Plant J. 2023:115(1):68–80. 10.1111/tpj.16209. PubMed DOI
Masel J, Siegal ML. Robustness: mechanisms and consequences. Trends Genet. 2009:25(9):395–403. 10.1016/j.tig.2009.07.005. PubMed DOI PMC
McCahill IW, Hazen SP. Regulation of cell wall thickening by a medley of mechanisms. Trends Plant Sci. 2019:24(9):853–866. 10.1016/j.tplants.2019.05.012. PubMed DOI
Meiklejohn CD, Hartl DL. A single mode of canalization. Trends Ecol Evol. 2002:17(10):468–473. 10.1016/S0169-5347(02)02596-X. DOI
Miranda C, Culp C, Škrabišová M, Joshi T, Belzile F, Grant D, Bilyeu K. Molecular tools for detecting Pdh1 can improve soybean breeding efficiency by reducing yield losses due to pod shatter. Mol Breeding. 2019:39(2):27. 10.1007/s11032-019-0935-1. DOI
Mitsuda N, Ohme-Takagi M. 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. 2008:56(5):768–778. 10.1111/j.1365-313X.2008.03633.x. PubMed DOI
Moghaddam SM, Mamidi S, Osorno JM, Lee R, Brick M, Kelly J, Miklas P, Urrea C, Song Q, Cregan P, et al. Genome-wide association study identifies candidate loci underlying agronomic traits in a middle American diversity panel of common bean. Plant Genome. 2016:9(3):1–21. 10.3835/plantgenome2016.02.0012. PubMed DOI
Murgia ML, Attene G, Rodriguez M, Bitocchi E, Bellucci E, Fois D, Nanni L, Gioia T, Albani DM, Papa R, et al. A comprehensive phenotypic investigation of the “pod-shattering syndrome” in common bean. Front Plant Sci. 2017:8:251. 10.3389/fpls.2017.00251. PubMed DOI PMC
Nelson AS, Gelambi M, Morales-M E, Whitehead SR. Fruit secondary metabolites alter the quantity and quality of a seed dispersal mutualism. Ecology. 2023:104(5):e4032. 10.1002/ecy.4032. PubMed DOI
Nelson AS, Whitehead SR. Fruit secondary metabolites shape seed dispersal effectiveness. Trends Ecol Evol. 2021:36(12):1113–1123. 10.1016/j.tree.2021.08.005. PubMed DOI
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015:32(1):268–274. 10.1093/molbev/msu300. PubMed DOI PMC
Ogutcen E, Pandey A, Khan MK, Marques E, Penmetsa RV, Kahraman A, Von Wettberg EJB. Pod shattering: a homologous series of variation underlying domestication and an avenue for crop improvement. Agronomy. 2018:8(8):137. 10.3390/agronomy8080137. DOI
Parker TA, Berny Mier Y Teran JC, Palkovic A, Jernstedt J, Gepts P. Pod indehiscence is a domestication and aridity resilience trait in common bean. New Phytol. 2020:225(1):558–570. 10.1111/nph.16164. PubMed DOI
Parker TA, de Sousa LL, de Oliveira Floriani T, Palkovic A, Gepts P. Toward the introgression of PvPdh1 for increased resistance to pod shattering in common bean. Theor Appl Genet. 2021:134(1):313–325. 10.1007/s00122-020-03698-7. PubMed DOI
Parker TA, Lo S, Gepts P. Pod shattering in grain legumes: emerging genetic and environment-related patterns. Plant Cell. 2021:33(2):179–199. 10.1093/plcell/koaa025. PubMed DOI PMC
Pérez-Antón M, Schneider I, Kroll P, Hofhuis H, Metzger S, Pauly M, Hay A. Explosive seed dispersal depends on SPL7 to ensure sufficient copper for localized lignin deposition via laccases. Proc Natl Acad Sci U S A. 2022:119(24):e2202287119. 10.1073/pnas.2202287119. PubMed DOI PMC
Pichersky E, Noel JP, Dudareva N. Biosynthesis of plant volatiles: nature's diversity and ingenuity. Science. 2006:311(5762):808. 10.1126/science.1118510. PubMed DOI PMC
Pourkheirandish M, Hensel G, Kilian B, Senthil N, Chen G, Sameri M, Azhaguvel P, Sakuma S, Dhanagond S, Sharma R, et al. Evolution of the grain dispersal system in barley. Cell. 2015:162(3):527–539. 10.1016/j.cell.2015.07.002. PubMed DOI
Qi X, Liu L, Liu C, Song L, Dong Y, Chen L, Li M. Sweet cherry AP2/ERF transcription factor, PavRAV2, negatively modulates fruit size by directly repressing PavKLUH expression. Physiol Plant. 2023:175(6):e14065. 10.1111/ppl.14065. PubMed DOI
Qiao X, Li Q, Yin H, Qi K, Li L, Wang R, Zhang S, Paterson AH. Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants. Genome Bio. 2019:20(1):38. 10.1186/s13059-019-1650-2. PubMed DOI PMC
R Core Team . R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; 2020. https://www.R-project.org/.
Rajani S, Sundaresan V. The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol. 2001:11(24):1914–1922. 10.1016/S0960-9822(01)00593-0. PubMed DOI
Rau D, Murgia ML, Rodriguez M, Bitocchi E, Bellucci E, Fois D, Albani D, Nanni L, Gioia T, Santo D, et al. Genomic dissection of pod shattering in common bean: mutations at non-orthologous loci at the basis of convergent phenotypic evolution under domestication of leguminous species. Plant J. 2019:97(4):693–714. 10.1111/tpj.14155. PubMed DOI
Ripoll JJ, Roeder AH, Ditta GS, Yanofsky MF. A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development. 2011:138(23):5167–5176. 10.1242/dev.073031. PubMed DOI
Rodríguez A, Alquézar B, Peña L. Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal. New Phytol. 2013:197(1):36–48. 10.1111/j.1469-8137.2012.04382.x. PubMed DOI
Selby R, Jones DS. Complex peptide hormone signaling in plant stem cells. Curr Opin Plant Biol. 2023:75:102442. 10.1016/j.pbi.2023.102442. PubMed DOI
Seo J-H, Kang B-K, Dhungana SK, Oh J-H, Choi M-S, Park J-H, Shin S-O, Kim H-S, Baek I-Y, Sung J-S, et al. QTL mapping and candidate gene analysis for pod shattering tolerance in soybean (Glycine max). Plants. 2020:9(9):1163. 10.3390/plants9091163. PubMed DOI PMC
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003:13(11):2498–2504. 10.1101/gr.1239303. PubMed DOI PMC
Sharma D, Koul A, Kaul S, Dhar MK. Tissue-specific transcriptional regulation and metabolite accumulation in tomato (Solanum lycopersicum L.). Protoplasma. 2020:257(4):1093–1108. 10.1007/s00709-020-01492-2. PubMed DOI
Shi Y, Li BJ, Su G, Zhang M, Grierson D, Chen KS. Transcriptional regulation of fleshy fruit texture. J Integr Plant Biol. 2022:64(9):1649–1672. 10.1111/jipb.13316. PubMed DOI
Smýkal P, Parker T. Domestication-related changes in seed dispersal and pigmentation: visual selection and functional trait? Mol Plant. 2023:16(8):1240–1242. 10.1016/j.molp.2023.07.007. PubMed DOI
Steigemann P, Gerlich DW. Cytokinetic abscission: cellular dynamics at the midbody. Trends Cell Biol. 2009:19(11):606–616. 10.1016/j.tcb.2009.07.008. PubMed DOI
Suzuki IK, Gacquer D, Van Heurck R, Kumar D, Wojno M, Bilheu A, Herpoel A, Lambert N, Cheron J, Polleux F, et al. Human-specific NOTCH2NL genes expand cortical neurogenesis through Delta/Notch regulation. Cell. 2018:173(6):1370–1384.e16. 10.1016/j.cell.2018.03.067. PubMed DOI PMC
Takahashi Y, Kongjaimun A, Muto C, Kobayashi Y, Kumagai M, Sakai H, Satou K, Teruya K, Shiroma A, Shimoji M, et al. Same locus for non-shattering seed pod in two independently domesticated legumes, Vigna angularis and Vigna unguiculata. Front Genet. 2020:11:748. 10.3389/fgene.2020.00748. PubMed DOI PMC
Tang D, Gallusci P, Lang Z. Fruit development and epigenetic modifications. New Phytol. 2020:228(3):839–844. 10.1111/nph.16724. PubMed DOI
Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH. Synteny and collinearity in plant genomes. Science. 2008:320(5875):486–488. 10.1126/science.1153917. PubMed DOI
Tohge T, Alseekh S, Fernie AR. On the regulation and function of secondary metabolism during fruit development and ripening. J Exp Bot. 2014:65(16):4599–4611. 10.1093/jxb/ert443. PubMed DOI
Vanholme R, De Meester B, Ralph J, Boerjan W. Lignin biosynthesis and its integration into metabolism. Curr Opin Biotechnol. 2019:56:230–239. 10.1016/j.copbio.2019.02.018. PubMed DOI
Wang D, Seymour GB. Molecular and biochemical basis of softening in tomato. Mol Hortic. 2022:2(1):5. 10.1186/s43897-022-00026-z. PubMed DOI PMC
Wang L, Liu X, Li Q, Xu N, He C. A lineage-specific arginine in POS1 is required for fruit size control in Physaleae (Solanaceae) via gene co-option. Plant J. 2022:111(1):183–204. 10.1111/tpj.15786. PubMed DOI
Wang W-N, Wei Y-T, Zhao S-T, Yu F-H, Wang J-W, Gu C-Y, Liu X-R, Sai N, Zhu J-L, Wang QM, et al. ABSCISIC ACID-INSENSITIVE 5-KIP-RELATED PROTEIN 1-SHOOT MERISTEMLESS modulates reproductive development of Arabidopsis. Plant Physiol. 2024:195(3):2309–2322. 10.1093/plphys/kiae146. PubMed DOI
Weeden NF. Genetic changes accompanying the domestication of Pisum sativum: is there a common genetic basis to the ‘domestication syndrome’ for legumes? Ann Bot. 2007:100(5):1017–1025. 10.1093/aob/mcm122. PubMed DOI PMC
Weeden NF, Brauner S, Przyborowski JA. Genetic analysis of pod dehiscence in pea (Pisum sativum L.). Cell Mol Biol Lett. 2002:7(2B):657–663. https://api.semanticscholar.org/CorpusID:13872236. PubMed
Wu H, He Q, He B, He S, Zeng L, Yang L, Zhang H, Wei Z, Hu X, Hu J, et al. Gibberellin signaling regulates lignin biosynthesis to modulate rice seed shattering. Plant Cell. 2023:35(12):4383–4404. 10.1093/plcell/koad244. PubMed DOI PMC
Wu H, He Q, Wang Q. Advances in rice seed shattering. Int J Mol Sci. 2023:24(10):8889. 10.3390/ijms24108889. PubMed DOI PMC
Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L, et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation (Camb). 2021:2(3):100141. 10.1016/j.xinn.2021.100141. PubMed DOI PMC
Xu B, Yang Z. PAMLX: a graphical user interface for PAML. Mol Biol Evol. 2013:30(12):2723–2724. 10.1093/molbev/mst179. PubMed DOI
Yang C, Song J, Ferguson AC, Klisch D, Simpson K, Mo R, Taylor B, Mitsuda N, Wilson ZA. Transcription factor MYB26 is key to spatial specificity in anther secondary thickening formation. Plant Physiol. 2017:175(1):333–350. 10.1104/pp.17.00719. PubMed DOI PMC
Yang JH, Wang H. Molecular mechanisms for vascular development and secondary cell wall formation. Front Plant Sci. 2016:7:356. 10.3389/fpls.2016.00356. PubMed DOI PMC
Yang SW, Jin E, Chung IK, Kim WT. Cell cycle-dependent regulation of telomerase activity by auxin, abscisic acid and protein phosphorylation in tobacco BY-2 suspension culture cells. Plant J. 2002:29(5):617–626. 10.1046/j.0960-7412.2001.01244.x. PubMed DOI
Yong B, Zhu W, Wei S, Li B, Wang Y, Xu N, Lu J, Chen Q, He C. Parallel selection of loss-of-function alleles of Pdh1 orthologous genes in warm-season legumes for pod indehiscence and plasticity is related to precipitation. New Phytol. 2023:240(2):863–879. 10.1111/nph.19150. PubMed DOI
Yuan L, Grotewold E. Plant specialized metabolism. Plant Sci. 2020:298:110579. 10.1016/j.plantsci.2020.110579. PubMed DOI
Zablatzká L, Balarynová J, Klčová B, Kopecký P, Smýkal P. Anatomy and histochemistry of seed coat development of wild (Pisum sativum subsp. elatius (M. Bieb.) Asch. et Graebn. and domesticated pea (Pisum sativum subsp. sativum L.). Int J Mol Sci. 2021:22(9):4602. 10.3390/ijms22094602. PubMed DOI PMC
Zeng JK, Li X, Xu Q, Chen JY, Yin XR, Ferguson IB, Chen KS. EjAP2-1, an AP2/ERF gene, is a novel regulator of fruit lignification induced by chilling injury, via interaction with EjMYB transcription factors. Plant Biotechnol J. 2015:13(9):1325–1334. 10.1111/pbi.12351. PubMed DOI
Zhai Y, Fan Z, Cui Y, Gu X, Chen S, Ma H. APETALA2/ethylene responsive factor in fruit ripening: roles, interactions and expression regulation. Front Plant Sci. 2022:13:979348. 10.3389/fpls.2022.979348. PubMed DOI PMC
Zhang QY, Tu BJ, Liu CK, Liu XB. Pod anatomy, morphology and dehiscing forces in pod dehiscence of soybean (Glycine max (L.) Merrill). Flora. 2018:248:48–53. 10.1016/j.flora.2018.08.014. DOI
Zhao Y, Zhang R, Jiang K-W, Qi J, Hu Y, Guo J, Zhu R, Zhang T, Egan AN, Yi T-S, et al. Nuclear phylotranscriptomics and phylogenomics support numerous polyploidization events and hypotheses for the evolution of rhizobial nitrogen-fixing symbiosis in Fabaceae. Mol Plant. 2021:14(5):748–773. 10.1016/j.molp.2021.02.006. PubMed DOI
Zhong R, Demura T, Ye Z-H. SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell. 2006:18(11):3158–3170. 10.1105/tpc.106.047399. PubMed DOI PMC
Zhou Y, Lu D, Li C, Luo J, Zhu B-F, Zhu J, Shangguan Y, Wang Z, Sang T, Zhou B, et al. Genetic control of seed shattering in rice by the APETALA2 transcription factor SHATTERING ABORTION1. Plant Cell. 2012:24(3):1034–1048. 10.1105/tpc.111.094383. PubMed DOI PMC