[en] Mendel1 studied in detail seven pairs of contrasting traits in pea (Pisum sativum), establishing the foundational principles of genetic inheritance. Here we investigate the genetic architecture that underlies these traits and uncover previously undescribed alleles for the four characterized Mendelian genes2-7, including a rare revertant of Mendel's white-flowered a allele. Primarily, we focus on the three remaining uncharacterized traits and find that (1) an approximately 100-kb genomic deletion upstream of the Chlorophyll synthase (ChlG) gene disrupts chlorophyll biosynthesis through the generation of intergenic transcriptional fusion products, conferring the yellow pod phenotype of gp mutants; (2) a MYB gene with an upstream Ogre element insertion and a CLE peptide-encoding gene with an in-frame premature stop codon explain the v and p alleles, which disrupt secondary cell wall thickening and lignification, resulting in the parchmentless, edible-pod phenotype; and (3) a 5-bp exonic deletion in a CIK-like co-receptor kinase gene, in combination with a genetic modifier locus, is associated with the fasciated stem (fa) phenotype. Furthermore, we characterize genes and alleles associated with diverse agronomic traits, such as axil ring anthocyanin pigmentation, seed size and the 'semi-leafless' form. This study establishes a foundation for fundamental research, education in biology and genetics, and pea breeding practices.
Disciplines :
Agriculture & agronomy
Author, co-author :
Feng, Cong ✱; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Chen, Baizhi ✱; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Hofer, Julie ✱; John Innes Centre, Norwich Research Park, Norwich, UK
Shi, Yan ✱; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Jiang, Mei ✱; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Song, Bo ; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Cheng, Hong; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Lu, Lu; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Wang, Luyao; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Howard, Alex; John Innes Centre, Norwich Research Park, Norwich, UK
Bendahmane, Abdel ; INRAE UMR 1403, Institute of Plant Sciences Paris-Saclay, Gif-sur-Yvette, France
Fouchal, Anissa; INRAE UMR 1403, Institute of Plant Sciences Paris-Saclay, Gif-sur-Yvette, France
Moreau, Carol; John Innes Centre, Norwich Research Park, Norwich, UK ; Paleogenomics Laboratory, INRAE Clermont-Auvergne-Rhône-Alpes, CS 60032, Clermont-Ferrand, France
Sawada, Chie; John Innes Centre, Norwich Research Park, Norwich, UK
LeSignor, Christine ; INRAE UMR1347-Agroecologie pôle GEAPSI, DIJON Cedex, France
Zhang, Cuijun ; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Vikeli, Eleni; John Innes Centre, Norwich Research Park, Norwich, UK
Tsanakas, Georgios; John Innes Centre, Norwich Research Park, Norwich, UK
Zhao, Hang ; Université de Liège - ULiège > TERRA Research Centre ; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Cheema, Jitender; John Innes Centre, Norwich Research Park, Norwich, UK ; EMBL-EBI, European Molecular Biology Laboratory, Wellcome Genome Campus, Hinxton, UK
Barclay, J Elaine; John Innes Centre, Norwich Research Park, Norwich, UK
Hou, Junliang; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Sayers, Liz; John Innes Centre, Norwich Research Park, Norwich, UK
Wingen, Luzie ; John Innes Centre, Norwich Research Park, Norwich, UK
Vigouroux, Marielle ; John Innes Centre, Norwich Research Park, Norwich, UK
Vickers, Martin ; John Innes Centre, Norwich Research Park, Norwich, UK
Ambrose, Mike; John Innes Centre, Norwich Research Park, Norwich, UK
Dalmais, Marion; INRAE UMR 1403, Institute of Plant Sciences Paris-Saclay, Gif-sur-Yvette, France
Higuera-Poveda, Paola; John Innes Centre, Norwich Research Park, Norwich, UK
Li, Pengfeng; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Yuan, Quan; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Spanner, Rebecca; John Innes Centre, Norwich Research Park, Norwich, UK ; Department of Plant Pathology, University of Minnesota, St Paul, MN, USA
Horler, Richard; John Innes Centre, Norwich Research Park, Norwich, UK
Wouters, Roland ; John Innes Centre, Norwich Research Park, Norwich, UK
Chundakkad, Smitha; John Innes Centre, Norwich Research Park, Norwich, UK
Wu, Tian; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Zhao, Xiaoxiao; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Li, Xiuli; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Sun, Yuchen; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Huang, Zejian; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Wu, Zhen; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Deng, Xing Wang ; State Key Laboratory of Wheat Improvement, School of Advanced Agricultural Sciences and School of Life Sciences, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China
Steuernagel, Burkhard ; John Innes Centre, Norwich Research Park, Norwich, UK
Domoney, Claire; John Innes Centre, Norwich Research Park, Norwich, UK
Ellis, Noel ✱; John Innes Centre, Norwich Research Park, Norwich, UK. Noel.Ellis2@jic.ac.uk
Chayut, Noam ; John Innes Centre, Norwich Research Park, Norwich, UK. Noam.Chayut@jic.ac.uk
Cheng, Shifeng ; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China. chengshifeng@caas.cn
The authors thank J. J. Doyle, M. Bennett, S. Huang, B. Lucas, D. Sanders and G. Moore for their invaluable support and comments for this project; colleagues for assistance in pea field trial and phenotyping work from experimental stations across northern and southern China; Y. Zhong and S. Liu; and L. Zhang for providing ZW1 genome assembly and annotation for comparison in this work; E. Jones and E. Crawford for plant phenotype data; M. Trick and S. Griffiths for valuable discussions at the John Innes Centre (JIC); the JIC NBI Computing Infrastructure for Science and JIC Bioinformatics groups for support in data handling and analysis; the JIC Field Trials and Horticultural Services teams for support with field and glasshouse experiments; the Molecular Genetics, Genotyping and DNA Extraction Platforms for support in experimental biology; and Bioimaging and Scientific Photography Platforms for phenotype visualization. This work was supported by the Program for Guangdong \u2018ZhuJiang\u2019 Introducing Innovative and Entrepreneurial Teams (2019ZT08N628), the National Natural Science Foundation of China (32022006), the Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2021-AGIS-ZDRW202101), the Shenzhen Science and Technology Program (AGIS-ZDKY202002), the National Key Research and Development Program of China (2023YFF1000100), and the National Key R&D Program of China (grant number 2023YFA0914600) to S. Cheng, and the National Natural Science Foundation of China (32401853) to Y. Shi. The work in the UK was possible due to the long-term investment of the UK Research Infrastructure Biotechnology and Biological Sciences Research Council (UKRI-BBSRC) through Institute Strategic Programme (ISP) grants, Institute Development Grant funds, and the Germplasm Resources National Capability Programme (BBS/E/J/000PR8000) and the National Bioscience Research Infrastructure grant (BBS/E/JI/23NB0001). We also acknowledge support from UKRI-BBSRC grants BB/J004561/1, BB/W510695/1 and BBS/E/J/000PR9799, the UK Department for Environment, Food, and Rural Affairs (Defra) through the Pulse Crop Genetic Improvement Network (grants CH0103 and CH0111) and the Provision and Maintenance of the Pea Genebank to Facilitate R&D Need grant (C5515), and JIC through its Institute Strategic Fund. We acknowledge the source of the TILLING mutant used in the analysis of gp as UMR1403-INRAE-IPS2, UMR1347-Agroecologie, France and the European Union FP6 Integrated Project Grain Legumes, FOOD-CT-2004-506223.
G. Mendel Versuche über plflanzenhybriden Verh. Naturforsch. Vereines Brünn 4 3 47
M.K. Bhattacharyya A.M. Smith T.H.N. Ellis C. Hedley C. Martin The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme Cell 60 115 122 1:CAS:528:DyaK3cXptlSntg%3D%3D 2153053 10.1016/0092-8674(90)90721-P
D.N. Martin W.M. Proebsting P. Hedden Mendel’s dwarfing gene: cDNAs from the le alleles and function of the expressed proteins Proc. Natl Acad. Sci. USA 94 8907 8911 1997PNAS..94.8907M 1:CAS:528:DyaK2sXltlWhtLs%3D 9238076 23192 10.1073/pnas.94.16.8907
I. Armstead et al. Cross-species identification of Mendel’s i locus Science 315 73 2007Sci..315..73A 1:CAS:528:DC%2BD28XhtlGqtL3P 17204643 10.1126/science.1132912
Y. Sato R. Morita M. Nishimura H. Yamaguchi M. Kusaba Mendel’s green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway Proc. Natl Acad. Sci. USA 104 14169 14174 2007PNAS.10414169S 1:CAS:528:DC%2BD2sXhtVWjtLjK 17709752 1955798 10.1073/pnas.0705521104
Y. Shimoda H. Ito A. Tanaka Arabidopsis stay-green, Mendel’s green cotyledon gene, encodes magnesium-dechelatase Plant Cell 28 2147 2160 1:CAS:528:DC%2BC28XitFSju7zE 27604697 5059807 10.1105/tpc.16.00428
R.P. Hellens et al. Identification of Mendel’s white flower character PLoS ONE 5 e13230 2010PLoSO..513230H 20949001 2952588 10.1371/journal.pone.0013230
J. Diamond Evolution, consequences and future of plant and animal domestication Nature 418 700 707 2002Natur.418.700D 1:CAS:528:DC%2BD38XlvVyltbY%3D 12167878 10.1038/nature01019
W.J. Dahl L.M. Foster R.T. Tyler Review of the health benefits of peas (Pisum sativum L.) Br. J. Nutr. 108 S3 S10 2012AJ..143..3D 1:CAS:528:DC%2BC38Xht1GjurfE 22916813 10.1017/S0007114512000852
V.E. Tsyganov A.V. Tsyganova Symbiotic regulatory genes controlling nodule development in Pisum sativum L Plants 9 1741 1:CAS:528:DC%2BB3MXktl2kur4%3D 33317178 7764586 10.3390/plants9121741
S. Abbott D.J. Fairbanks Experiments on plant hybrids by Gregor Mendel Genetics 204 407 422 27729492 5068836 10.1534/genetics.116.195198
T.H.N. Ellis J.M.I. Hofer M.T. Swain P.J. van Dijk Mendel’s pea crosses: varieties, traits and statistics Hereditas 156 33 31695583 6823958 10.1186/s41065-019-0111-y
Franklin, A. What Makes a Good Experiment? (Univ. Pittsburgh Press, 2016).
P. Smýkal et al. Pea (Pisum sativum L.) in the genomic era Agronomy 2 74 115 10.3390/agronomy2020074
O.E. White The present state of knowledge of heredity and variation in peas Proc. Am. Phil. Soc. 56 487 588
J. Kreplak et al. A reference genome for pea provides insight into legume genome evolution Nat. Genet. 51 1411 1422 1:CAS:528:DC%2BC1MXhs12nsrnI 31477930 10.1038/s41588-019-0480-1
T. Yang et al. Improved pea reference genome and pan-genome highlight genomic features and evolutionary characteristics Nat. Genet. 54 1553 1563 1:CAS:528:DC%2BB38XisVKns7fM 36138232 9534762 10.1038/s41588-022-01172-2
K. Shirasawa K. Sasaki H. Hirakawa S. Isobe Genomic region associated with pod color variation in pea (Pisum sativum) G3 11 jkab081 1:CAS:528:DC%2BB38Xhs1yht7bN 33720317 8104947 10.1093/g3journal/jkab081
P. Zhang et al. Fine mapping PsPS1, a gene controlling pod softness that defines market type in pea (Pisum sativum) Plant Breed 141 418 428 1:CAS:528:DC%2BB38Xht1ens7rK 10.1111/pbr.13020
N. Liu et al. Reference genome sequence and population genomic analysis of peas provide insights into the genetic basis of Mendelian and other agronomic traits Nat. Genet. 56 1964 1974 1:CAS:528:DC%2BB2cXhslWlurvK 39103648 10.1038/s41588-024-01867-8
H. De Beukelaer G.F. Davenport V. Fack Core hunter 3: flexible core subset selection BMC Bioinformatics 19 203 29855322 6092719 10.1186/s12859-018-2209-z
R. Jing et al. The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis BMC Evol. Biol. 10 44 20156342 2834689 10.1186/1471-2148-10-44
S.R. Turner D.H.P. Barratt R. Casey The effect of different alleles at the r locus on the synthesis of seed storage proteins in Pisum sativum Plant Mol. Biol. 14 793 803 1:CAS:528:DyaK3cXksFGqtLY%3D 2102857 10.1007/BF00016512
D.N. Price C.M. Smith C.L. Hedley The effect of the gp gene on fruit development in Pisum sativum L. I. Structural and physical aspects New Phytol. 110 261 269 1:CAS:528:DyaL1MXnt1KnsQ%3D%3D 10.1111/j.1469-8137.1988.tb00261.x
M. Dalmais et al. Utilldb, a Pisum sativum in silicoforward and reverse genetics tool Genome Biol. 9 R43 18302733 2374714 10.1186/gb-2008-9-2-r43
Ruel, J. De Natura Stirpium Libri Tres (Froben Press, Basel, 1537).
H. Ram N.K. Hedau G.V. Chaudhari L. Kant Peas with zero shelling edible pods: a review Sci. Hortic. 288 110333 10.1016/j.scienta.2021.110333
H. Yaginuma Y. Hirakawa Y. Kondo K. Ohashi-Ito H. Fukuda A novel function of TDIF-related peptides: promotion of axillary bud formation Plant Cell Physiol. 52 1354 1364 1:CAS:528:DC%2BC3MXhtVeiu7vO 21693505 10.1093/pcp/pcr081
Y. Ito et al. Dodeca-CLE peptides as suppressors of plant stem cell differentiation Science 313 842 845 2006Sci..313.842I 1:CAS:528:DC%2BD28XnvVynt7o%3D 16902140 10.1126/science.1128436
J.P. Etchells S.R. Turner The PXY–CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division Development 137 767 774 1:CAS:528:DC%2BC3cXksVChu7g%3D 20147378 10.1242/dev.044941
Y. Hirakawa et al. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system Proc. Natl Acad. Sci. USA 105 15208 15213 2008PNAS.10515208H 1:CAS:528:DC%2BD1cXht1aqtbfI 18812507 2567516 10.1073/pnas.0808444105
K. Fisher S. Turner Pxy, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development Curr. Biol. 17 1061 1066 1:CAS:528:DC%2BD2sXmsFKnt7o%3D 17570668 10.1016/j.cub.2007.05.049
M.E. Smit et al. A PXY-mediated transcriptional network integrates signaling mechanisms to control vascular development in arabidopsis Plant Cell 32 319 335 1:CAS:528:DC%2BB3cXltFCmu7w%3D 31806676 10.1105/tpc.19.00562
J.P. Etchells M.E. Smit A. Gaudinier C.J. Williams S.M. Brady A brief history of the TDIF‐PXY signalling module: balancing meristem identity and differentiation during vascular development New Phytol. 209 474 484 1:CAS:528:DC%2BC2MXitV2jtrrI 26414535 10.1111/nph.13642
Karaca, D. E. Molecular Mapping of the v Locus in Pea (Pisum sativum l.). Master of Science Thesis, Washington State Univ. (2019).
Y. Yang et al. The pea R2R3-MYB gene family and its role in anthocyanin biosynthesis in flowers Front. Genet. 13 936051 1:CAS:528:DC%2BB38XitFejsrjN 35873471 9299958 10.3389/fgene.2022.936051
Yang, C. at al. Transcription factor MYB26 is key to spatial specificity in anther secondary thickening formation. Plant Physiol.175, 333–350 (2017).
T.A. Parker S. Lo P. Gepts Pod shattering in grain legumes: emerging genetic and environment-related patterns Plant Cell 33 179 199 33793864 8136915 10.1093/plcell/koaa025
Gerard, J. The Herball, or, Generall Historie of Plantes (John Norton, 1597).
A.A. Sinjushin S.A. Gostimsky Fasciation in pea: basic principles of morphogenesis Russ. J. Dev. Biol. 37 375 381 10.1134/S1062360406060063
A. Sinjushin S. Gostimskii Relationship between different fasciated lines of pea Pisum Genetics 39 16 18
C. Hu et al. A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis Nat. Plants 4 205 211 1:CAS:528:DC%2BC1cXmtVCktrY%3D 29581511 10.1038/s41477-018-0123-z
M.A. Osipova et al. WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of cle peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation Plant Physiol. 158 1329 1341 1:CAS:528:DC%2BC38XltVOksbg%3D 22232385 3291250 10.1104/pp.111.188078
S. Blixt Mutation genetics in Pisum Agric. Hort. Genet. 30 1 293
P.J. van Dijk A.P. Jessop T.H.N. Ellis How did Mendel arrive at his discoveries? Nat. Genet. 54 926 933 35817970 10.1038/s41588-022-01109-9
N.W. Albert A.G. Griffiths G.R. Cousins I.M. Verry W.M. Williams Anthocyanin leaf markings are regulated by a family of R2R3‐MYB genes in the genus Trifolium New Phytol. 205 882 893 1:CAS:528:DC%2BC2cXitFansbjJ 25329638 10.1111/nph.13100
C. Wang et al. The antagonistic MYB paralogs RH1 and RH2 govern anthocyanin leaf markings in Medicago truncatula New Phytol. 229 3330 3344 1:CAS:528:DC%2BB3MXnvVCqtLk%3D 33222243 10.1111/nph.17097
N. Ellis et al. Recombinant inbred lines derived from wide crosses in pisum Sci. Rep. 13 20408 20408 2023NatSR.1320408E 1:CAS:528:DC%2BB2cXhvFelsrnF 37990072 10663473 10.1038/s41598-023-47329-9
N.A. Ramsay B.J. Glover MYB–bHLH–WD40 protein complex and the evolution of cellular diversity Trends Plant Sci. 10 63 70 1:CAS:528:DC%2BD2MXhtlajtrg%3D 15708343 10.1016/j.tplants.2004.12.011
C. Sawada et al. An integrated linkage map of three recombinant inbred populations of pea (Pisum sativum L) Genes 13 196 196 1:CAS:528:DC%2BB38XlslSltL0%3D 35205241 8871737 10.3390/genes13020196
I. D’Erfurth et al. A role for an endosperm-localized subtilase in the control of seed size in legumes New Phytol. 196 738 751 22985172 10.1111/j.1469-8137.2012.04296.x
D. Yi et al. The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species Plant Cell 26 296 309 1:CAS:528:DC%2BC2cXks1Snsr0%3D 24399300 3963576 10.1105/tpc.113.118943
N. Tayeh et al. afila, the origin and nature of a major innovation in the history of pea breeding New Phytol. 243 15 10.1111/nph.19800
J. Burstin et al. Developmental genes have pleiotropic effects on plant morphology and source capacity, eventually impacting on seed protein content and productivity in pea Plant Physiol. 144 768 781 1:CAS:528:DC%2BD2sXmvValtro%3D 17449650 1914171 10.1104/pp.107.096966
R. Olby Mendel no Mendelian? Hist. Sci. 17 53 72 10.1177/007327537901700103
K. Kampourakis Mendel and the path to genetics: Portraying science as a social process Sci. Educ. 22 293 324 10.1007/s11191-010-9323-2
R.A. Fisher Has Mendel’s work been rediscovered? Ann. Sci. 1 115 137 10.1080/00033793600200111
S. Cheng Gregor Mendel: the father of genetics who opened a biological world full of wonders Mol. Plant 15 1641 1645 36262045 10.1016/j.molp.2022.10.013
A. Stoltzfus J.M. Logsdon J.D. Palmer W.F. Doolittle Intron “sliding” and the diversity of intron positions Proc. Natl Acad. Sci. USA 94 10739 10744 1997PNAS..9410739S 1:CAS:528:DyaK2sXmtlekt7g%3D 9380704 23469 10.1073/pnas.94.20.10739
D.H. Huson D. Bryant Application of phylogenetic networks in evolutionary studies Mol. Biol. Evol. 23 254 267 1:CAS:528:DC%2BD28XntValsw%3D%3D 16221896 10.1093/molbev/msj030
Rayner, T. et al. Rebalancing the seed proteome following deletion of vicilin-related genes in pea (Pisum sativum L.). J. Exp. Bot.https://doi.org/10.1093/jxb/erae518 (2024).
H. Li R. Durbin Fast and accurate short read alignment with Burrows–Wheeler transform Bioinformatics 25 1754 1760 1:CAS:528:DC%2BD1MXot1Cjtbo%3D 19451168 2705234 10.1093/bioinformatics/btp324
H. Li et al. The Sequence Alignment/Map format and SAMtools Bioinformatics 25 2078 2079 19505943 2723002 10.1093/bioinformatics/btp352
M.A. DePristo et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data Nat. Genet. 43 491 498 1:CAS:528:DC%2BC3MXksFWguro%3D 21478889 3083463 10.1038/ng.806
Freed, D, Aldana, R, Weber, J. A. & Edwards, J. S. The Sentieon Genomics Tools—a fast and accurate solution to variant calling from next-generation sequence data. Preprint at BioRxiv https://doi.org/10.1101/115717 (2017).
P. Cingolani et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff Fly 6 80 92 1:CAS:528:DC%2BC38Xht1GmtL3E 22728672 3679285 10.4161/fly.19695
W. Wang et al. Genomic variation in 3,010 diverse accessions of Asian cultivated rice Nature 557 43 49 2018Natur.557..43W 1:CAS:528:DC%2BC1cXovVWrsr0%3D 29695866 6784863 10.1038/s41586-018-0063-9
S. Purcell et al. PLINK: a tool set for whole-genome association and population-based linkage analyses Am. J. Hum. Genet. 81 559 575 1:CAS:528:DC%2BD2sXhtVSqurrL 17701901 1950838 10.1086/519795
S.R. Browning B.L. Browning Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering Am. J. Hum. Genet. 81 1084 1097 1:CAS:528:DC%2BD2sXht1KmsL3M 17924348 2265661 10.1086/521987
C. Feng et al. HAPPE: a tool for population haplotype analysis and visualization in editable Excel tables Front. Plant Sci. 13 927407 35845648 9284118 10.3389/fpls.2022.927407
K. Schneeberger Using next-generation sequencing to isolate mutant genes from forward genetic screens Nat. Rev. Genet. 15 662 676 1:CAS:528:DC%2BC2cXhtlyls7nL 25139187 10.1038/nrg3745
N.A.-F. Aboul-Maaty H.A.-S. Oraby Extraction of high-quality genomic DNA from different plant orders applying a modified CTAB-based method Bull. Natl. Res. Cent. 43 25 10.1186/s42269-019-0066-1
X. Zhou M. Stephens Genome-wide efficient mixed-model analysis for association studies Nat. Genet. 44 821 824 1:CAS:528:DC%2BC38Xos12gur0%3D 22706312 3386377 10.1038/ng.2310
J. He et al. An innovative procedure of genome-wide association analysis fits studies on germplasm population and plant breeding Theor. Appl. Genet. 130 2327 2343 1:CAS:528:DC%2BC2sXhtlKmsbrK 28828506 10.1007/s00122-017-2962-9
C. Domoney et al. Exploiting a fast neutron mutant genetic resource in Pisum sativum (pea) for functional genomics Funct. Plant Biol. 40 1261 1:CAS:528:DC%2BC3sXhslyqt7bM 32481193 10.1071/FP13147
M. Grønlund A. Olsen E.I. Johansen I. Jakobsen Protocol: using virus-induced gene silencing to study the arbuscular mycorrhizal symbiosis in Pisum sativum Plant Methods 6 28 21156044 3018388 10.1186/1746-4811-6-28
X. Li et al. BIGGER ORGANS and ELEPHANT EAR-LIKE LEAF1 control organ size and floral organ internal asymmetry in pea J. Exp. Bot. 70 179 191 1:CAS:528:DC%2BC1MXisVGmsbbI 30295864 10.1093/jxb/ery352
G.D. Constantin et al. Virus‐induced gene silencing as a tool for functional genomics in a legume species Plant J. 40 622 631 1:CAS:528:DC%2BD2cXhtVyit7jJ 15500476 10.1111/j.1365-313X.2004.02233.x
P.B. Brewer M.G. Heisler J. Hejátko J. Friml E. Benková In situ hybridization for mRNA detection in Arabidopsis tissue sections Nat. Protoc. 1 6 10.1038/nprot.2006.226
M.I. Love W. Huber S. Anders Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biol. 15 550 25516281 4302049 10.1186/s13059-014-0550-8
D.H. Alexander J. Novembre K. Lange Fast model-based estimation of ancestry in unrelated individuals Genome Res. 19 1655 1664 1:CAS:528:DC%2BD1MXhtFCjsLvL 19648217 2752134 10.1101/gr.094052.109
C. Zhang S.-S. Dong J.-Y. Xu W.-M. He T.-L. Yang PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files Bioinformatics 35 1786 1788 1:CAS:528:DC%2BC1MXit1eku7jM 30321304 10.1093/bioinformatics/bty875
H. Zhang X. Lin Z. Han L.-J. Qu J. Chai Crystal structure of PXY–TDIF complex reveals a conserved recognition mechanism among CLE peptide–receptor pairs Cell Res. 26 543 555 1:CAS:528:DC%2BC28XlvVanu7c%3D 27055373 4856767 10.1038/cr.2016.45
T.H.N. Ellis et al. Diversity of pod shape in Pisum Diversity 13 203 2021ahlf.book...E 10.3390/d13050203
V.A. Berdnikov et al. The neoplastic pod gene (Np) may be a factor for resistance to the pest Bruchus pisorum L Pisum Genet. 24 3
A. Sinjushin A. Liberzon Contribution to genetic control of flower number in pea (Pisum sativum L.) Ratar. Povrt. 53 4
J.L. Weller et al. A conserved molecular basis for photoperiod adaptation in two temperate legumes Proc. Natl Acad. Sci. USA 109 21158 21163 2012PNAS.10921158W 1:CAS:528:DC%2BC3sXmvFOnsA%3D%3D 23213200 3529011 10.1073/pnas.1207943110
J. Balarynová et al. The loss of polyphenol oxidase function is associated with hilum pigmentation and has been selected during pea domestication New Phytol. 235 1807 1821 35585778 10.1111/nph.18256