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Phylogeny, phylogeography and genetic diversity of the Pisum genus

Published online by Cambridge University Press:  17 November 2010

Petr Smýkal ,
Gregory Kenicer ,
Andrew J. Flavell ,
Jukka Corander ,
Oleg Kosterin ,
Robert J. Redden ,
Rebecca Ford ,
Clarice J. Coyne ,
Nigel Maxted  and
Mike J. Ambrose
...Show all authors
Petr Smýkal*
Affiliation:
Agritec Plant Research Limited, Department of Biotechnology, Zemedelská 2520/16, CZ-787 01 Šumperk, Czech Republic
Gregory Kenicer
Affiliation:
Royal Botanic Garden Edinburgh, Edinburgh EH3 5LR, UK
Andrew J. Flavell
Affiliation:
Division of Plant Sciences, University of Dundee at SCRI, Invergowrie, Dundee DD2 5DA, UK
Jukka Corander
Affiliation:
Department of Mathematics, Abo Akademi University, Biskopsgatan 8, FIN-20500 Åbo, Finland
Oleg Kosterin
Affiliation:
Institute of Cytology and Genetics, Siberian Department of Russian Academy of Sciences, 630090 Novosibirsk, Russia
Robert J. Redden
Affiliation:
Australian Temperate Field Crops Collection, Horsham VIC 3401, Australia
Rebecca Ford
Affiliation:
Melbourne School of Land and Environment, The University of Melbourne, Victoria 3010, Australia
Clarice J. Coyne
Affiliation:
USDA – Agricultural Research Service, WSU, Pullman WA99164, USA
Nigel Maxted
Affiliation:
School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK
Mike J. Ambrose
Affiliation:
John Innes Centre, Colney, Norwich NR4 7UH, UK
Noel T. H. Ellis
Affiliation:
John Innes Centre, Colney, Norwich NR4 7UH, UK
*
*Corresponding author. E-mail: [email protected]
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Abstract

The tribe Fabeae (formerly Vicieae) contains some of humanity's most important grain legume crops, namely Lathyrus (grass pea/sweet pea/chickling vetches; about 160 species); Lens (lentils; 4 species); Pisum (peas; 3 species); Vicia (vetches; about 140 species); and the monotypic genus Vavilovia. Reconstructing the phylogenetic relationships within this group is essential for understanding the origin and diversification of these crops. Our study, based on molecular data, has positioned Pisum genetically between Vicia and Lathyrus and shows it to be closely allied to Vavilovia. A study of phylogeography, using a combination of plastid and nuclear markers, suggested that wild pea spread from its centre of origin, the Middle East, eastwards to the Caucasus, Iran and Afghanistan, and westwards to the Mediterranean. To allow for direct data comparison, we utilized model-based Bayesian Analysis of Population structure (BAPS) software on 4429 Pisum accessions from three large world germplasm collections that include both wild and domesticated pea analyzed by retrotransposon-based markers. An analysis of genetic diversity identified separate clusters containing wild material, distinguishing Pisum fulvum, P. elatius and P. abyssinicum, supporting the view of separate species or subspecies. Moreover, accessions of domesticated peas of Afghan, Ethiopian and Chinese origin were distinguished. In addition to revealing the genetic relationships, these results also provided insight into geographical and phylogenetic partitioning of genetic diversity. This study provides the framework for defining global Pisum germplasm diversity as well as suggesting a model for the domestication of the cultivated species. These findings, together with gene-based sequence analysis, show that although introgression from wild species has been common throughout pea domestication, much of the diversity still resides in wild material and could be used further in breeding. Moreover, although existing collections contain over 10,000 pea accessions, effort should be directed towards collecting more wild material in order to preserve the genetic diversity of the species.

Keywords

Bayesian inferencecore collectiondomesticationgenetic diversitygermplasmmicrosatellitepeaphylogenyPisumretrotransposon
Type
Research Article
Information
Plant Genetic Resources , Volume 9 , Issue 1 , April 2011 , pp. 4 - 18
Copyright
Copyright © NIAB 2010

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References

Ambrose, MJ (1995) From Near East centre of origin the prized pea migrates throughout world. Diversity 11: 118–119.Google Scholar
Ascheron, P and Graebner, P (1910) Synopsis der mitteleuropaischen Flora Bd 6, Abt 2, IV Leipzig 1093 S.Google Scholar
Aubert, G, Morin, J, Jacquin, F, Loridon, K, Quillet, MC, Petit, A, Rameau, C, Lejeune-He'naut, I, Huguet, T and Burstin, J (2009) Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume. Medicago truncatula. Theoretical and Applied Genetics 112: 1024–1041.CrossRefGoogle Scholar
Baranger, AG, Aubert, G, Arnau, G, Lainé, AL, Deniot, G, Potier, J, Weinachter, C, Lejeune-Hénaut, J, Lallemand, J and Burstin, J (2004) Genetic diversity within Pisum sativum using protein- and PCR-based markers. Theoretical and Applied Genetics 108: 1309–1321.CrossRefGoogle ScholarPubMed
Beaumont, MA and Rannala, B (2004) The Bayesian revolution in genetics. Nature Reviews in Genetics 5: 251–261.CrossRefGoogle ScholarPubMed
Ben-Ze'ev, N and Zohary, D (1973) Species relationship in the genus Pisum L. Israel Journal of Botany 22: 73–91.Google Scholar
Berger, A (1928) Systematic botany of peas and their allies. In: Hedrick, U (ed.) The Vegetables of New York. 1. Albany: State of New York, Education Department, pp. 10–18.Google Scholar
Bhargava, A and Fuentes, FF (2010) Mutational dynamics of microsatellites. Molecular Biotechnology 44: 250–266.CrossRefGoogle ScholarPubMed
Bieberstein, M (1808) Flora taurico-caucasica exhibens stirpes phaenomagas, in Chersoneso Taurica et regionibus caucasicis sponte crescentes. Bd 2 Charkouiae, Typ Akad 477 S.Google Scholar
Bogdanova, VS (2007) Inheritance of organelle DNA markers in a pea cross associated with nuclear-cytoplasmic incompatibility. Theoretical and Applied Genetics 114: 333–339.Google Scholar
Bogdanova, VS, Galieva, ER and Kosterin, OE (2009) Genetic analysis of nuclear-cytoplasmic incompatibility in pea associated with cytoplasm of an accession of wild subspecies Pisum sativum subsp. elatius (Bieb.) Schmahl. Theoretical and Applied Genetics 118: 801–809.CrossRefGoogle ScholarPubMed
Boissier, E (1856) Diagnoses plantarum orientalum novarum. Lipsie 3: 125.Google Scholar
Breese, EL (1989) Regeneration and Multiplication of Germplasm Resources in Seed Genebanks: The Scientific Background. Rome: International Board for Plant Genetic Resources.Google Scholar
Brown, AHD and Spillane, C (1999) Implementing core collections-principles, procedures, progress, problems and promise. In: Johnson, RC and Hodgkin, T (eds) Core Collections for Today and Tomorrow. Rome, Italy: International Plant Genetic Resources Institute, pp. 1–9.Google Scholar
Burstin, J, Deniot, G, Potier, J, Weinachter, C, Aubert, G and Baranger, A (2001) Microsatellite polymorphism in Pisum sativum. Plant Breeding 120: 311–317.Google Scholar
Cieslarová, J, Smýkal, P, Dočkalová, Z, Hanáček, P, Procházka, S, Hýbl, M and Griga, M (2010) Molecular evidence of genetic diversity changes in pea (Pisum sativum L.) germplasm after long-term maintenance. Genetic Resources and Crop Evolution. doi 10.1007/s10722-010-9591-3.Google Scholar
Corander, J and Martiinen, P (2006) Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15: 2833–2843.CrossRefGoogle ScholarPubMed
Corander, J, Waldmann, P and Sillanpää, MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 164: 367–374.CrossRefGoogle Scholar
Corander, J, Waldmann, P, Marttinen, P and Sillanpää, MJ (2004) BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20: 2363–2369.CrossRefGoogle ScholarPubMed
Corander, J, Gyllenberg, M and Koski, T (2007) Random partition models and exchangeability for Bayesian identification of population structure. The Bulletin of Mathematical Biology 69: 797–815.CrossRefGoogle ScholarPubMed
Coyne, CJ, Brown, A, Timmerman-Vaughan, GM, McPhee, KE and Grusak, MA (2005) Refined USDA-ARS pea core collection based on 26 quantitative traits. Pisum Genetics 37: 3–6.Google Scholar
Davis, PH (1970) Pisum L. In: Davis, PH (ed.) Flora of Turkey and East Aegean Islands. vol. 3. Edinburg: Edinburg University Press, pp. 370–373.Google Scholar
Deulvot, C, Charrel, H, Marty, A, Jacquin, F, Donnadieu, C, Lejeune-Hénaut, I, Burstin, J and Aubert, G (2010) Highly-multiplexed SNP genotyping for genetic mapping and germplasm diversity studies in pea. BMC Genomics 11: 468.CrossRefGoogle ScholarPubMed
Doyle, JJ, Doyle, JL, Ballenger, JA, Dickson, EE, Kajita, T and Ohashi, (1997) A phylogeny of the chloroplast gene rbcL in the Leguminosae: taxonomic correlations and insights into the evolution of nodulation. American Journal of Botany 84: 541–554.CrossRefGoogle ScholarPubMed
Ellis, THN and Poyser, SJ (2002) An integrated and comparative view of pea genetic and cytogenetic maps. New Phytologist 153: 17–25.CrossRefGoogle Scholar
Ellis, THN, Poyser, SJ, Knox, MR, Vershinin, AV and Ambrose, MJ (1998) Polymorphism of insertion sites of Ty1-copia class retrotransposons and its use for linkage and diversity analysis in pea. Molecular and General Genetics 260: 9–19.Google Scholar
Endo, Y, Choi, BH, Ohashi, H and Delgado-Salinas, A (2008) Phylogenetic relationships of New World Vicia (Leguminosae) inferred from nrDNA internal transcribed spacer sequences and floral characters. Systematic Botany 33: 356–363.CrossRefGoogle Scholar
Falush, D, Stephens, M and Pritchard, JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.CrossRefGoogle ScholarPubMed
Ford, R, Le Roux, K, Itman, C, Brouwer, JB and Taylor, PWJ (2002) Genome-specific sequence tagged microsatellite site (STMS) markers for diversity analysis and genotyping in Pisum species. Euphytica 124: 397–405.CrossRefGoogle Scholar
Furman, BJ, Ambrose, M, Coyne, CJ and Redden, B (2006) Formation of PeaGRIC: an international consortium to co-ordinate and utilize the genetic diversity and agro ecological distribution of major collections of Pisum. Pisum Genetics 38: 32–34.Google Scholar
Govorov, LI (1937) Goroch (Peas). Kulturnaja Flora SSR (in Russian). Moscow: State Printing Office, pp. 229–336.Google Scholar
Hodgkin, T, Brown, AHD and van Hintum, TJL and Morales, EAV (eds) (1995) Core Collections of Plant Genetic Resources. Chichester: John Wiley & Sons, pp. 95–107.Google Scholar
Hoey, BK, Crowe, KR, Jones, VM and Polans, NO (1996) A phylogenetic analysis of Pisum based on morphological characters, allozyme and RAPD markers. Theoretical and Applied Genetics 92: 92–100.CrossRefGoogle ScholarPubMed
Hu, J, Zhu, J and Xu, HM (2000) Methods of constructing core collections by stepwise clustering with three sampling strategies based on the genotypic valued of crops. Theoretical and Applied Genetics 101: 264–268.Google Scholar
Huelsenbeck, JP, Ronquist, F, Nielsen, R and Bollback, JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310–2314.Google Scholar
Jing, RC, Knox, MR, Lee, JM, Vershinin, AV, Ambrose, M, Ellis, THN and Flavell, AJ (2005) Insertional polymorphism and antiquity of PDR1 retrotransposon insertions in Pisum species. Genetics 171: 741–752.CrossRefGoogle ScholarPubMed
Jing, R, Johnson, R, Seres, A, Kiss, G, Ambrose, MJ, Knox, MR, Ellis, TH and Flavell, AJ (2007) Gene-based sequence diversity analysis of field pea (Pisum). Genetics 177: 2263–2275.Google Scholar
Jing, R, Vershinin, A, Grzebyta, J, Shaw, P, Smýkal, P, Marshall, D, Ambrose, MJ, Ellis, THN and Flavell, AJ (2010) The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evolutionary Biology 10: 44.Google Scholar
Kalendar, R and Schulman, AH (2006) IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nature Protocols 1: 2478–2484.Google Scholar
Kass, E and Wink, M (1996) Molecular evolution of the Leguminosae: phylogeny of the three subfamilies based on rbcL-sequences. Biochemical Systematics and Ecology 24: 365–378.Google Scholar
Kenicer, GJ (2007) Systematics and biogeography of Lathyrus L. (Leguminosae, papilionoideae). PhD Thesis, Royal Botanical Garden Edinburgh.Google Scholar
Kenicer, G, Smýkal, P and Mikič, A (2008) Phylogenetic study of mysterious Vavilovia formosa (Stev.) Fed., a Pisum relative. IV. International Conference on Legume Genetics and Genomics, 2008 Puerto Vallarta, Mexico, pp. 83.Google Scholar
Kenicer, GJ, Kajita, T, Pennington, RT and Murata, J (2005) Systematics and biogeography of Lathyrus (Leguminosae) based on internal transcribed spacer and cpDNA sequence data. American Journal of Botany 92: 1199–1209.CrossRefGoogle ScholarPubMed
Knight, TA (1799) Experiments on the Fecundation of Vegetables. Philosophical Transactions of the Royal Society 89: 504–509.Google Scholar
Kosterin, OE and Bogdanova, VS (2008) Relationship of wild and cultivated forms of Pisum L. as inferred from an analysis of three markers, of the plastid, mitochondrial and nuclear genomes. Genetic Resources and Crop Evolution 55: 735–755.Google Scholar
Kosterin, OE, Zaytseva, OO, Bogdanova, VS and Ambrose, M (2010) New data on three molecular markers from different cellular genomes in Mediterranean accessions reveal new insights into phylogeography of Pisum sativum L. subsp elatius (Bieb.) Schmalh. Genetic Resources and Crop Evolution 57: 733–739.CrossRefGoogle Scholar
Kupicha, FK (1981) Vicieae (Adans.) DC. (1825) nom conserv prop. In: Polhill, RM and Raven, PH (eds) Advances in Legume Systematics 1. Kew: Royal Botanical Gardens, pp. 377–381.Google Scholar
Lamprecht, H (1963) Zur Kenntnis von Pisum arvense L. oect. abyssinicum Braun, mit genetischen und zytologischen Ergebnissen. Agric Hort Genetics 21: 35–55.Google Scholar
Lamprecht, H (1966) Die Enstehung der Arten und hoheren Kaategorien. Wien: Springer Verlag.Google Scholar
Latch, EK, Dharmarajan, G, Glaubitz, JC and Rhodes, OE (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conservation Genetics 7: 295–302.Google Scholar
Lavin, M, Herendeen, PS and Wojciechowski, M (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Systematic Biology 54: 575–594.Google Scholar
Lee, D, Ellis, THN, Turner, L, Hellens, RP and Cleary, WG (1990) A copia-like element in Pisum demonstrates the uses of dispersed repeated sequences in genetic-analysis. Plant Molecular Biology 15: 707–722.CrossRefGoogle ScholarPubMed
Lee, MJ, Davenport, GF, Marshall, D, Ellis, THN, Ambrose, MJ, Dicks, J, van Hintum, TJL and Flavell, AJ (2005) GERMINATE. A generic database for integrating genotypic and phenotypic information for plant genetic resource collections. Plant Physiology 139: 619–631.Google Scholar
Lehmann, C (1954) Das morphologische system der Saaterbsen. Der Zuchter 24: 316–337.Google Scholar
Lewis, G, Schrirer, B, Mackinder, B and Lock, M (eds) (2005) Legumes of the World. Kew: Royal Botanical Gardens.Google Scholar
Lock, M and Maxted, N (2005) Tribe Fabeae. In: Lewis, G, Schrire, B, Mackinder, B and Lock, M (eds) Legumes of the World. Richmond: Royal Botanic Gardens, Kew.Google Scholar
Macas, J, Neumann, P and Navrátilová, A (2007) Repetitive DNA in the pea (Pisum sativum L. genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8: 427.CrossRefGoogle ScholarPubMed
Makasheva, RK (1979) Gorokh (pea). In: Korovina, ON (ed.) Leningrad: Kulturnaya Flora SSR, Kolos, pp. 1–324 (in Russian).Google Scholar
Marx, GA (1977) Classification, genetics and breeding. In: Sutcliffe, JF and Pate, JS (eds) Physiology of the Garden Pea. New York: Academic Press, pp. 21–43.Google Scholar
Maxted, N and Ambrose, N (2000) Peas (Pisum L.) Chapter 10. In: Maxted, N and Bennett, SJ (eds) Plant Genetic Resources of Legumes in the Mediterranean. Dordrecht: Kluwer Academic Publishers, pp. 181–190.Google Scholar
Maxted, N, Hargreaves, S, Kell, SP, Amri, A, Street, K, Shehadeh, A, Piggin, J and Konopka, J (2010) Temperate forage and pulse legume genetic gap analysis. Paper given at XIII OPTIMA Meeting in Antalya, Turkey, 22–26 March 2010.Google Scholar
Mendel, JG (1866) Versuche über Pflanzen-Hybriden. Verhandlungen des Naturforschenden Vereins in Brünn 4: 3–47. (see also http://www.mendelweb.org/).Google Scholar
Miller, P (1768) The Gardener's Dictionary; Containing the Methods of Cultivating and Improving the Kitchen, Fruit and Flower Garden. etc. printed by J. and J. Rivington, Reprint 1969, Verlag von J. Cramer, Germany, 8th ed. London.Google Scholar
Nasiri, J, Haghnazari, A and Saba, J (2009) Genetic diversity among varieties and wild species accessions of pea (Pisum sativum L.) based on SSR markers. African Journal of Biotechnology 15: 3405–3417.Google Scholar
Ochatt, SJ, Benabdelmouna, A, Marget, P, Aubert, G, Moussy, F, Pontecaille, C and Jacas, L (2004) Overcoming hybridization barriers between pea and some of its wild relatives. Euphytica 137: 353–359.CrossRefGoogle Scholar
Palmer, JD, Jorgensen, RA and Thompson, WF (1985) Chloroplast DNA variation and evolution in Pisum: patterns of change and phylogenetic analysis. Genetics 109: 195–213.Google Scholar
Pearce, SR, Knox, M, Ellis, TH, Flavell, AJ and Kumar, A (2000) Pea Ty1-copia group retrotransposons: transpositional activity and use as markers to study genetic diversity in Pisum. Molecular and General Genetics 263: 898–907.Google Scholar
Polans, NO and Saar, DE (2002) ITS sequence variation in wild species and cultivars of pea. Pisum Genetics 34: 9–13.Google Scholar
Pritchard, JK, Stephens, M and Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.Google Scholar
Raquin, AL, Depaulis, F, Lambert, A, Galic, N, Brabant, P and Goldringer, I (2008) Experimental estimation of mutation rates in a wheat population with a gene genealogy approach. Genetics 179: 2195–2211.CrossRefGoogle Scholar
Rosenberg, NA (2002) Genetic structure of human populations. Science 298: 2381–2002.Google Scholar
Saar, DE and Polans, NO (2000) ITS sequence variation in selected taxa of Pisum. Pisum Genetics 109: 195–213.Google Scholar
Sáenz de Miera, LE, Ramos, J and Pérez de la Vega, M (2008) A comparative study of convicilin storage protein gene sequences in species of the tribe Vicieae. Genome 7: 511–523.Google Scholar
Schmalhausen, I (1895) Flora Srednei y Yuzhnoj Rossii, Kryma i Severnogo Kavkaza. 1: 468 (in Russian).Google Scholar
Smýkal, P (2006) Development of an efficient retrotransposon-based fingerprinting method for rapid pea variety identification. Journal of Applied Genetics 47: 221–230.Google Scholar
Smýkal, P, Hýbl, M, Corander, J, Jarkovský, J, Flavell, A and Griga, M (2008 a) Genetic diversity and population structure of pea (Pisum sativum L.) varieties derived from combined retrotransposon, microsatellite and morphological marker analysis. Theoretical and Applied Genetics 117: 413–424.Google Scholar
Smýkal, P, Coyne, CJ, Ford, R, Redden, R, Flavell, AJ, Hýbl, M, Warkentin, T, Burstin, J, Duc, G, Ambrose, M and Ellis, THN (2008 b) Effort towards a world pea (Pisum sativum L.) germplasm core collection: the case for common markers and data compatibility. Pisum Genetics 40: 11–14.Google Scholar
Smýkal, P, Kenicer, G and Mikič, A (2009 a) Beautiful Vavilovia (Vavilovia formosa) and molecular taxonomy of tribe Fabeae. Book of Abstracts IV Congress of the Serbian Genet Society, p. 166.Google Scholar
Smýkal, P, Kalendar, R, Ford, R, Macas, J and Griga, M (2009 b) Evolutionary conserved lineage of Angela-like retrotransposons as a genome-wide microsatellite repeat dispersal agent. Heredity 103: 157–167.Google Scholar
Steele, KP and Wojciechowski, MF (2003) Phylogenetic analyses of tribes Trifolieae and Vicieae, based on sequences of the plastid gene matK (Papilionoideae: Leguminosae). In: Klitgaard, BB and Bruneau, (eds) Advances in Legume Systematics. Kew: Royal Botanical Garden, pp. 355–370.Google Scholar
Tar'an, B, Zhang, C, Warkentin, T, Tullu, A and Vandenberg, A (2005) Genetic diversity among varieties and wild species accessions of pea (Pisum sativum L.) based on molecular markers, and morphological and physiological characters. Genome 48: 257–272.Google Scholar
Thachuk, C, Crossa, J, Franco, J, Dreisigacker, S, Warburton, M and Davenport, GF (2009) Core hunter: an algorithm for sampling genetic resources based on multiple genetic measures. BMC Bioinformatics 10: 243.Google Scholar
Van Hintum, TJL (1999) The general methodology for creating a core collection. In: Johnson, RC and Hodgkin, T (eds) Core Collections for Today and Tomorrow. Rome: International Plant Genetic Resources Institute, pp. 10–17.Google Scholar
Vershinin, AV, Allnutt, TR, Knox, MR, Ambrose, MJ and Ellis, NTH (2003) Transposable elements reveal the impact of introgression, rather than transposition, in Pisum diversity, evolution, and domestication. Molecular Biology and Evolution 20: 2067–2075.CrossRefGoogle ScholarPubMed
Vigouroux, Y, Jaqueth, JS, Matsuoka, Y, Smith, OS, Beavis, WD, Smith, JSC and Doebley, J (2002) Rate and pattern of mutation at microsatellite loci in maize. Molecular Biology and Evolution 19: 1251–1260.CrossRefGoogle ScholarPubMed
Wang, JC, Hu, J, Xu, HM and Zhang, S (2007) A strategy on constructing core collections by least distance stepwise sampling. Theoretical and Applied Genetics 115: 1–8.CrossRefGoogle ScholarPubMed
Westphal, E (1974) Pulses in Ethiopia, their taxonomy and agricultural significance. Versl Landbouwkundl Onderzoek. The Netherlands: Wageningen.Google Scholar
Wojciechowski, MF, Lavin, M and Sanderson, MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. American Journal of Botany 91: 1846–1862.Google Scholar
Young, JPW and Matthews, P (1982) A distinct class of peas (Pisum sativum L.) from Afghanistan that show strain specificity for symbiotic Rhizobium. Heredity 48: 203–210.CrossRefGoogle Scholar
Zohary, D and Hopf, M (2000) Domestication of Plants in the Old World. Oxford: Oxford University Press.Google Scholar
Zong, X, Redden, RJ, Liu, Q, Wang, S, Guan, J, Liu, J, Xu, Y, Liu, X, Gu, J, Yan, L, Ades, P and Ford, R (2009) Analysis of a diverse global Pisum sp. collection and comparison to a Chinese local collection with microsatellite markers. Theoretical and Applied Genetics 118: 193–204.CrossRefGoogle ScholarPubMed