Pea (Pisum sativum L.): the uneasy fate of the first genetical object. O. E. Kosterin

Abstract:

Pea (Pisum sativum L.) is an important vegetable and forage crop capable of improving soils via symbiotic nitrogen fixation. It is of special importance in Russia as a crop adapted to high latitudes and an inexpensive source of plant protein. In addition, pea is the first genetical object used in famous G. Mendel’s experiments. The first translocation in the history of genetics was also found in pea. Pea generation time can be shortened to 35 days, which is comparable with Arabidopsis. However, small and hardly recognizable chromosomes hampered the development of pea cytogenetics, while recombination genetic maps remained inadequate until 1990s, when they were improved only with the aid of molecular methods. Two different notations for pea linkage groups and chromosomes as cytological objects still coexist. Recently, the whole toolbox of modern molecular methods of genetic analysis was applied to pea, including isozymes, RAPD-, SSR-, RFLP-, AFLP-, STS-, CAPS-, sCAPS-, and SNP-markers, as well as methods of reverse genetics including TILLING and virus-induced genomic silencing. Application of association mapping. Several transcriptome studies have been carried out in pea. Meanwhile, we await the completion of pea nuclear genome sequencing in 2016. For working out new molecular markers in pea, the synteny of its genome to the sequenced genome of Medicago truncatula is extensively used. Genetic transformation of pea is very difficult. Pea has been used as an experimental model for investigation of the following fundamental issues: the genetic control of symbiosis with nitrogen fixing bacteria, influence of variation in the histone H1 gene on the phenotype, mechanism of nuclear- cytoplasmic conflict in remote crosses, origin of B-chromosomes in plants, and genetic control of compound leaf morphology.

About The Author:

O. E. Kosterin. Institute of Cytology and Genetics SB RAS, Novosibirsk, Russia; Novosibirsk State University, Novosibirsk, Russia, Russian Federation

References:

1. Berdnikov V.A., Bogdanova V.S., Rozov S.M., Kosterin O.E. Formirovanie mnogoobraziya genov gistona N1 v khode kul’turnoĭ evolyutsii gorokha. Vavilovskoe nasledie v sovremennoĭ biologii. M.: Nauka, 1989:72-89.

2. Bogdanova V.S., Galieva E.R. Narusheniya meĭoza kak proyavlenie yaderno-tsitoplazmaticheskoĭ nesovmestimosti pri skreshchivanii podvidov posevnogo gorokha. Genetika. 2009;45(5):711-716.

3. Bogdanova V.S., Kosterin O.E. Sluchaĭ anomal’nogo nasledovaniya khloroplastov v skreshchivaniyakh posevnogo gorokha s uchastiem odnoĭ iz dikikh form. Dokl. AN. 2006;406(2):256-259.

4. Borisov A.Yu., Shtark O.Yu., Zhukov V.A., Naumkina T.S., Pinaev A.G., Akhmetova G.A., Voroshilova V.A., Ovchinnikova E.S., Rychagova T.S., Tsyganov V.E., Zhernakov A.I., Kuznetsova E.V., Grishina O.A., Sulima A.S., Fedorina Ya.V., Chebotar’ V.K., O.E. Bisseling T., Lemanso F., Dzhianinazi-Pirson V., Rate P., Sankhuan Kh., Stougaard Ĭ., Berg G., Makfi K., Ellis N., Tikhonovich I.A. Vzaimodeĭstvie bobovykh s poleznymi pochvennymi organizmami: ot genov rasteniĭ k sortam. S.-kh. biologiya. 2011;3:41-47.

5. Genetika — selektsii rasteniĭ. Raĭonirovannye sorta i perspektivnye formy sel’skokhozyaĭstvennykh rasteniĭ Instituta tsitologii i genetiki SO AN SSSR za 30 let. Prospekt (Red. V.K. Shumnyĭ). Novosibirsk, 1987.

6. Dal’ V.I. Tolkovyĭ slovar’ zhivogo velikorusskogo yazyka. M.: Rus. yazyk, 1955;1.

7. Kosterin O.E., Bogdanova V.S., Gorel’ F.L., Berdnikov V.A. Trisomiki gorokha (Pisum sativum L.) demonstriruyut legkiĭ otvet na otbor na povyshenie plodovitosti. Dokl. AN. 2008;423(3):417-420.

8. Levitskiĭ G.A. Morfologiya khromosom. Tr. po prikl. botan., genet. i selektsii. 1931;27:103-173.

9. Lutkov A.N. Mezhvidovye gibridy Pisum humile Boiss. × Pisum sativum L. Tr. Vsesoyuz. kongr. po genetike, selektsii i semenovodstvu. L., 1930;2:353-365.

10. Rozov S.M., Bogdanova V.S., Berdnikov V.A. Razlichiya v khromosomnoĭ lokalizatsii genov, kodiruyushchikh fraktsii gistona N1 gorokha. Genetika. 1986;22:2159-2166.

11. Tikhonovich I.A., Provorov N.A. Razvitie podkhodov simbiogenetiki dlya izucheniya izmenchivosti i nasledstvennosti nadvidovykh sistem. Genetika. 2012;48:437.

12. Fuchzhun L., Gostimskiĭ S.A. Issledovaniya translokatsiĭ u gorokha. Genetika. 1998;34(9):1269-1276.

13. Yurchenko N.N., Ivannikov A.V., Zakharov I.K. Istoriya otkrytiĭ na drozofile — etapy razvitiya genetiki. Vavilovskiĭ zhurnal genetiki i selektsii. 2015;19(1):39-49.

14. Yakovlev G.P. Bobovye zemnogo shara. L.: Nauka, 1991.

15. Aubert G., Morin J., Jacquin F., Loridon K., Quillet M.C., Petit A., Rameau C., Lejeune-Hénaut I., Huguet T., Burstin J. Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume. Medicago truncatula. Theor. Appl. Genet. 2006;112:1024-1041.

16. Baranger A.G., Aubert G., Arnau G., Lainé A.L., Deniot G., Potier J., Weinachter C., Lejeune-Hénaut I., Lallemand J., Burstin J. Genetic diversity within Pisum sativum using protein — and PCR based markers. Theor. Appl. Genet. 2004;108:1309-1321.

17. Bastianelli D., Grosjean F., Peyronnet C., Duparque M., Regnier J.M. Feeding value of pea (Pisum sativum, L.). 1. Chemical composition of different categories of pea. Anim. Sci. 1998;67:609-619.

18. Berdnikov V.A., Bogdanova V.S., Gorel F.L., Kosterin O.E., Trusov Y.A. Large changes in the structure of the major histone H1 subtype result in small effects on quantitative traits in legumes. Genetica. 2003a;119:167-182.

19. Berdnikov V.A., Bogdanova V.S., Rozov S.M., Kosterin O.E. Geographic patterns of histone H1 allelic frequencies formed in the course of Pisum sativum L. (pea) cultivation. Heredity. 1993a;71:199-209.

20. Berdnikov V.A., Gorel F.L. A mutation, tl2, in pea (Pisum sativum L.) affects leaf development only in the heterozygous state. Theor. Appl. Genet. 2005;110:1086-1091.

21. Berdnikov V.A., Gorel F.L. Combination of mutations sil and ins2 can cause conversion of stipules into compound leaves. Pisum Genet. 2004;36:3-5.

22. Berdnikov V.A., Gorel F.L. Tl2, a new locus resembling Tl in action. Pisum Genet. 2001;33:1-4.

23. Berdnikov V.A., Gorel F.L., Bogdanova V.S., Kosterin O.E. Interaction of a new leaf mutation ins2 with af, unitac and tlw. Pisum Genet. 2000;32:9-12.

24. BerdnikovV.A.,GorelF.L.,BogdanovaV.S.,KosterinO.E.,TrusovY.A., Rozov S.M. Effect of a substitution of a short chromosome segment carrying a histone H1 locus on expression of the homeiotic gene Tl in heterozygote in the garden pea Pisum sativum L. Genet. Res. 1999a;70:93-109.

25. Berdnikov V.A., Gorel F.L., Kosterin O.E. Two simultaneously induced lethal mutations provide a system for automatic reproduction of a heterozygote for the Hammarlund translocation. Pisum Genet. 1999b;31:1-4.

26. Berdnikov V.A., Gorel F.L., Kosterin O.E., Bogdanova V.S. Tertiary trisomics in the garden pea as a model of B chromosome evolution in plants. Heredity. 2003b;91:577-583.

27. Berdnikov V.A., Rozov S.M., Temnykh S.V., Gorel’ F.L., Kosterin O.E. Adaptive nature of interspecies variation of histone H1 in insects. J. Mol. Evol. 1993b;36:497-507.

28. Blixt S. Cytology of Pisum. II. The normal karyotype. Agr. Hortique Genet. 1958;16:221-237.

29. Blixt S. Mutation genetics in Pisum. Agr. Hortique Genet. 1972;30: 1-294.

30. Bogdanova V.S. Inheritance of organelle DNA markers in a pea cross associated with nuclear-cytoplasmic incompatibility. Theor. Appl. Genet. 2007;114:333-339.

31. Bogdanova V.S., Berdnikov V.A. Observation of the phenomenon resembling hybrid dysgenesis in a wild pea subspecies Pisum sativum ssp. Elatius. Pisum Genet. 2001;33:5-8.

32. Bogdanova V.S., Galieva E.R., Kosterin O.E. Genetic analysis of nuclear-cytoplasmic incompatibility in pea associated with cytoplasm of an accession of wild subspecies Pisum sativum subsp. elatius (Bieb.) Schmahl. Theor. Appl. Genet. 2009;118:801-809.

33. Bogdanova V.S., Galieva E.R., Yadrikhinskiy A.K., Kosterin O.E. Inheritance and genetic mapping of two nuclear genes involved in nuclear-cytoplasmic incompatibility in peas (Pisum sativum L.). Theor. Appl. Genet. 2012;124:1503-1512.

34. Bogdanova V.S., Kosterin O.E., Berdnikov V.A. Phenotypic effect of substitution of allelic variants for a histone H1 subtype specific for growing tissues in the garden pea (Pisum sativum L.). Genetica. 2007;130:61-72.

35. Bogdanova V.S., Kosterin O.E., Yadrikhinskiy A.K. Wild peas vary in their cross-compatibility with cultivated pea (Pisum sativum subsp. sativum L.) depending on alleles of a nuclear-cytoplasmic incompatibility locus. Theor. Appl. Genet. 2014;127:1163-1172.

36. Bogdanova V.S., Rozov S.M., Trusov Y.A., Berdnikov V.A. Phenotypic effect of substitutions of short chromosomal segments containing different alleles of histone H1 genes in garden pea (Pisum sativum L.). Genet. Res. 1994;64:35-41.

37. Bogdanova V.S., Zaytseva O.O., Mglinets A.V., Shatskaya N.V., Kosterin O.E. , Vasiliev G.V. Nucleic-cytoplasmic conflict in pea (Pisum sativum L.) is associated with nuclear and plastidic genes encoding Acetyl-CoA carboxylase subunits. PLoS One. 2015;10(3). 10.1371/journal.pone.0119835

38. Bordat A., Savois V., Nicolas M., Salse J., Chauveau A., Bourgeois M., Potier J., Houtin H., Rond C., Murat F., Marget P., Aubert G., Burstin J. Translational genomics in legumes allowed placing in silico 5460 unigenes on the pea functional map and identified candidate genes in Pisum sativum L. G3: Genes, Genomes, Genetics. 2011;1:93-103.

39. Bourgeois M., Jacquin F., Savois V., Sommerer N., Labas V., Henry C., Burstin J. Dissecting the proteome of pea mature seeds reveals the phenotypic plasticity of seed protein composition. Proteomics. 2009;9:254-271.

40. Bourgeois M., Jacquin F., Cassecuelle F., Savois V., Belghazi M., Aubert G., Quillien L., Huart M., Marget P., Burstin J. A PQL (protein quantity loci) analysis of mature pea seed proteins identifies loci determining seed protein composition. Proteomics. 2011;9:1581-1594.

41. Burton R.S., Pereira R.J., Barreto F.S. Cytonuclear genomic interactions and hybrid breakdown. Ann. Rev. Ecol. Evol. Syst. 2013;44:281-302.

42. Carrillo E., Satovic Z., Aubert G., Boucherot K., Rubiales D., Fondevilla S. Identification of quantitative trait loci and candidate genes for specific cellular resistance responses against Didymella pinodes in pea. Plant Cell Rep. 2014;33:1133-1345.

43. Castillejo M.A., Amiour N., Gaudot E.D., Rubiales D., Jorrín J.V. A proteomic approach to studying plant response to crenate broomrape (Orobanche crenata) in pea (Pisum sativum). Phytochemistry. 2004;65:1817-1828.

44. Castillejo M.A., Curto M., Fondevilla S., Rubiales D., Jorrín J.V. Two-dimensional electrophoresis based proteomic analysis of the pea (Pisum sativum) in response to Mycosphaerella pinodes. J. Agric. Food Chem. 2010;58:12822-12832.

45. Champagne C.E.M., Goliber C.E., Wojciechowski M.F., Mei R.W., Townsley B.T., Wang K., Paz M.M., Geeta R., Sinha N.R. Compound leaf development and evolution in the legumes. Plant Cell. 2007;19:3369-3378.

46. Cheghamirza K., Koveza O., Konovalov F., Gostimsky S. Identification of RAPD markers and their use for molecular mapping in pea (Pisum sativum L.). Cell. Mol. Biol. Lett. 2002;7:649-655.

47. Choi H.K., Mun J.H., Kim D.J., Zhu H., Baek J.M., Mudge J., Roe B., Ellis N., Doyle J., Kiss G.B., Young N.D., Cook D. Estimating genome conservation between crop and model legume species. Proc. Natl Acad. Sci. USA. 2004;101:15289-15294.

48. Constantin G.D., Krath B.N., MacFarlane S.A., Nicolaisen M., Johansen I.E., Lund O.S. Virus-induced gene silencing as a tool for functional genomics in a legume species. Plant J. 2004;40:622-631.

49. Couzigou J.M., Zhukov V., Mondy S., el Heba G.A., Cosson V., Ellis T.N., Ambrose M., Wen J., Tadege M., Tikhonovich I., Mysore T.S., Putterill J., Hofer J., Borisov A., Ratet P. NODULE ROOT and COCHLEATA maintain nodule development and are legume orthologs of Arabidopsis BLADE-ON-PETIOLE genes. Plant Cell. 2012;24:4498-4510.

50. Coyne C.J., McClendon M.T., Walling J.G., Timmerman-Vaughan G.M., Murray S., Meksem K., Lightfoot D.A., Shultz, J.L., Keller K.E., Martin R.R., Inglis D.A., Rajesh P.N., McPhee K.E., Weeden N.F., Grusak N.A., Li C.-M., Storlie E.W. Construction and characterization of two bacterial artificial chromosome libraries of pea (Pisum sativum L.) for the isolation of economically important genes. Genome. 2007;50:871-875.

51. Curto M., Camafeita E., Lopez J.A., Maldonado A.M., Rubiales D., Jorrín J.V. A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi). Proteomics. 2006;6: S163-S174.

52. Dalmais M., Schmidt J., Le Signor C., Moussy F., Burstin J., Savois V., Aubert G., Brunaud V., de Oliveira Z., Guichard C., Thompson R., Bedahmane A. UTILLdb, a Pisum sativum in silico forward and reverse genetics tool. Genome Biol. 2008;9:43. DOI: 10.1186/gb2008-9-2-r43

53. De Martino T., Errico A., Lassandro A., Conicella C. Distorting segregation resulting from pea chromosome reconstruction with alien segments from Pisum fulvum. J. Hered. 2000;91:322-325.

54. Decarie J., Coyne C., Brumett S., Shultz J. Additional pea EST-SSR markers for comparative mapping in pea (Pisum sativum L.). Plant Breed. 2012;131:222-226.

55. Deulvot C., Charrel H., Marty A., Jacquin F., Donnadieu C., LejeuneHénaut I., Burstin J., Aubert G. Highly-multiplexed SNP genotyping for genetic mapping and germplasm diversity studies in pea. BMC Genomics. DOI: ;11.DOI:10.1186/1471-2164-11-468

56. Dolezel J., Greilhuber J. Nuclear genome size. Are we getting closer? Cytometry. 2010;77:635-642.

57. Duarte J., Rivière N., Baranger A., Aubert G., Burstin J., Cornet L., Lavaud C., Lejeune-He′naut I., Martinant J.P., Pichon J.P., PiletNayel M.L., Boutet G. Transcriptome sequencing for high throughput SNP development and genetic mapping in pea. BMC Genomics. 2014;Feb 12;15:126. DOI: 10.1186/1471-2164-15-126

58. Dumont E., Bahrman N., Goulas E., Valot B., Sellier H., Hilbert J.L., Lejeune-Hénaut I., Delbreil B. A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci. 2011;180:86-98.

59. Ellis T.H.N., Hellens R.P., Turner L., Lee C., Domoney C., Welham T. On the pea lilnkage group. Pisum Genetics. 1993;25:5-12.

60. Ellis T.H.N., Poyser S.J. An integrated and comparative view of pea genetic and cytogenetic maps. New Phytol. 2002;153:17-25.

61. Ellis T.H.N., Poyser S.J., Knox M.R., Vershinin A.V., Ambrose M.J. Polymorphism of insertion sites of Ty1-copia class retrotransposons and its use for linkage and diversity analysis in pea. Mol. Gen. Genet. 1998;260:9-19.

62. Ferguson B.J., Reid J.B. Cochleata: getting to the root of legume nodules. Plant Cell Physiol. 2005;49:1583-1589.

63. Folkeson D. Assignment of linkage segments to chromosomes 3 and 5 in Pisum sativum L. Hereditas. 1990a;112:249-255.

64. Folkeson D. Assignment of linkage segments to chromosomes 4 and 7 in Pisum sativum L. Hereditas. 1990b;112:257-263.

65. Folkeson D. The use of BSG-staining in making a more detailed nomenclature possible for interchange systems in Pisum sativum L. Hereditas. 1984a;101:119-122.

66. Folkeson D. Free segregation between a (3S-7S) interchange and genes within linkage group VII in Pisum sativm L. Hereditas,1984b;101:127-133.

67. Franssen S.U., Shrestha R.P., Brätigam A., Bronberg-Bauer E., Wever A.P.M. Comprehensive transcriptome analysis of the highly complex Pisum sativum genome using next generation sequencing. BMC Genomics. 2011;12:277.

68. Fuchs J., Kühne M., Schubert I. Assignment of linkage groups to pea chromosomes after karyotyping and gene mapping by fluorescent in situ hybridization. Chromosoma. 1998;107:272-276.

69. Gilpin B.J., McCallum J.A., Frew T.J., Timmerman-Vaughan G.M. A linkage map of the pea (Pisum sativum L.) genome containing cloned sequences of known function and expressed sequence tags (ESTs). Theor. Appl. Genet. 1997;95:1289-1299.

70. Gorel F.L., Berdnikov V.A., Kosterin O.E. Mutation air dots (adt) with slight unitac-like effect on the leaf. Pisum Genet. 2002;34:1-2. Gourlay C.W., Hofer J.M.I., Ellis T.H.N. Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, COCHLEATA, AFILA, and TENDRIL-LESS. Plant Cell. 2000;12:1279-1294.

71. Greilhuber J., Ebert I. Genome size variation in Pisum sativum. Genome. 1994;37:646-655.

72. Gronlund M., Olsen A., Johansen I.E., Jakobsen I. Protocol: Using virus-induced gene silencing to study the arbuscular mycorrhizal symbiosis in Pisum sativum. Plant Methods. 2010;6. DOI: 10.1186/1746-4811-6-28

73. Hall K.J., Parker J.S., Ellis T.H. The relationship between genetic and cytogenetic maps of pea. I. Standard and translocation karyotypes. Genome. 1997;40:744-754.

74. Håkansson A. Chromosomenringe in Pisum und ihre Mutmassliche Genetische Bedeutung. Hereditas. 1929;12:1-10.

75. Hammarlund A. Über einen Fall von Koppelung und freie Kombination bei Erbsen. Hereditas. 1923;4:235-238.

76. Hellens R.P., Moreau C., Lin-Wang K., Schwinn K.E., Thomson S.J., Fiers M.W.E.J., Frew T.J., Murray S.R., Hofer J.M.I., Jacobs J.M.E.,O.E. Davies K.M., Allan A.C., Bendahmane A. Identification of Mendel’s white flower character. PLoS One. 2010;5. Art. e1323. DOI: 10.1371/journal.pone.0013230

77. Hoey B.K., Crowe K.R., Jones V.M., Polans N.O. A phylogenetic analysis of Pisum based on morphological characters, and allozyme and RAPD markers. Theor. Appl. Genet. 1996;92:92-100.

78. Hofer J., Turner L., Moreau C., Ambrose M., Isaac P., Butcher S., Weller J., Dupin A., Dalmais M., Le Signor C., Bendahmane A., Ellis N. Tendril-less regulates tendril formation in pea leaves. Plant Cell. 2009;21:420-428.

79. Hofer J.M.J., Ellis T.H.N. The effect of Uni on leaf shape. Pisum Genet. 1996;28:21-22.

80. Husbands A., Emirzade T., DeMason D. Stipulae morphologies of the sinuate leaf (sil) mutants. Pisum Genet. 2003;35:6-9.

81. Jing R., Johnson R., Seres A., Kiss G., Ambrose M.J., Knox M.R., Ellis T.H.N., Flavell A.J. Gene-based sequence diversity analysis of field pea (Pisum). Genetics. 2007;177:2263-2275.

82. Jing R., Vershinin A., Grzebota J., Shaw P., Smýkal P., Marshall D., Ambrose M.J., Ellis T.H.N., Flavell A.J. The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evol. Biol. 2010;10. Art. 44

83. Kaló P., Seres A., Taylor S.A., Jakab J., Kevei Z., Kereszt A., Endre G., Ellis T.H.N., Kiss G.B. Comparative mapping between Medicago sativa and Pisum sativum. Molecular and General Genomics. 2004;272:235-246.

84. Keller K.E., Johansen E., Martin R.R., Hampton R.O. Potyvirus genome-linked protein (VPg) determines pea seed-borne mosaic virus pathotype-specific virulence in Pisum sativum. Mol. PlantMicrobe Interactions. 1998;11:124-130.

85. Knox M.R., Ellis T.H.N. Stability and inheritance of methylation states at PstI sites in Pisum. Mol. Genet. Genomics. 2001;265: 497-507.

86. Knox M.R., Ellis T.H.N. Excess heterozygosity contributes to genetic map expansion in pea recombinant inbred populations. Genetics. 2002;162:861-873.

87. Konovalov F.A., Toshchakova E., Gostimsky S. A CAPS marker set for mapping in linkage group III of pea (Pisum sativum L.). Cell. Mol. Biol. Lett. 2005;10:163-171.

88. Kosterin O.E. Mapping of the third locus for histone H1 genes in peas. Pisum Genet. 1992;24:56-59.

89. Kosterin O.E. Genes a and d may not be in the same linkage group. Pisum Genet. 1993;25:23-26.

90. Kosterin O.E., Bogdanova V.S. Reciprocal compatibility within the genus Pisum L. as studied in F1 hybrids: 1. Crosses involving P. sativum L. subsp. Sativum. Genet. Res. Crop Evol. 2014. DOI:10.1007/s10722-014-0189z(E-pub ahead of print).

91. Kosterin O.E., Bogdanova V.S., Gorel F.L., Rozov S.M., Trusov Yu.A., Berdnikov V.A. Histone H1 of the garden pea (Pisum sativum L.): composition, developmental changes, allelic polymorphism and inheritance. Plant Sci. 1994;101:189-202.

92. Kosterin O.E., Bogdanova V.S., Kechin A.A., Zaytseva O.O., Yadrikhinskiy A.K. Polymorphism in a histone H1 subtype with a short N-terminal domain in three legume species (Fabaceae, Fabaeae). Mol. Biol. Rep. 2012;39:10681-10695.

93. Kosterin O.E., Rozov S.M. Mapping of the new mutation blb and the problem of integrity of linkage group 1. Pisum Genet. 1993;25: 27-31.

94. Lamm R. Cytogenetical studies on translocations in Pisum. Hereditas. 1951;37:356-372.

95. Lamm R. Transpositions in Pisum. Pisum Newslett. 1977;9:28-29. Lamm R., Miravalle R.J. A translocation tester set in Pisum. Hereditas. 1959;45:417-440.

96. Lamprecht H. The variation in linkage and course of crossingover. Agr. Hortique Genet. 1948;6:10-48.

97. Lamprecht H. Further studies on the interchange between the chromosomes III and V of Pisum. Agr. Hortique Genet. 1953;11:141-148.

98. Lamprecht H. Die Koppelung des Gens wsp und die Genenkarte von Chromosom VII von Pisum. Agr. Hortique Genet. 1954;12:115120.

99. Lamprecht H. Ein Interchange zwischen den Chromosomen I and VII von Pisum. Agr. Hortique Genet. 1955;13:173-182.

100. Lamprecht H. Die Genenkarte von Chromosom VI und das Interchange der Chromosomen IV/VI von Pisum. Agr. Hortique Genet. 1957;15:115-141.

101. Lamprecht H. Die Genenkarte von Pisum. Agr. Hortique Genet. 1961;19:360-401.

102. Laucou V., Haurogne K., Ellis N., Rameau C. Genetic mapping in pea. I. RAPD-based linkage map of Pisum sativum. Theor. Appl. Genet. 1998;97:905-915.

103. Loridon K., McPhee K.E., Morin J., Dubreuil P., Pilet-Nayel M.L., Aubert G., Rameau C., Baranger A., Coyne C.J., Lejeune-Hénault I., Burstin C. Microsatellite marker polymorphism and mapping in pea (Pisum sativum L.). Theor. Appl. Genet. 2005;111:1022-1031.

104. Lu J., Knox M.R., Ambrose M.J., Brown J.K.M., Ellis T.H.N. Comparative analysis of genetic diversity in pea assessed by RFLPand PCR-based methods. Theor. Appl. Genet. 1996;93:1103-1111.

105. Macas J., Neumann P., Návratilová A. Repetitive DNA in the pea (Pisum sativum L.) genome: Comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics. 2007;8. Art. 427

106. Magee A.M., Aspinall S., Rice D.W., Cusack B.P., Sémon M., Perry A.S., Stefanović S., Milbourne D., Barth S., Palmer J.D., Gray J.C., Kavanagh T.A., Wolfe K.H. Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Res. 2010;20:1700-1710.

107. Mendel G. Versuche über Plflanzenhybriden. Verhandlungen des naturforschenden Vereines in Brünn. Bd. IV für das Jahr1865 (Abhandlungen). 1866;3-47.

108. Murfet I.C. The gi locus shows linkage with gp, r and tl. Pisum Newstlett. 1990;22:38-40.

109. Neumann P., Nouzová M., Macas J. Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.). Genome 2001;44:716-728.

110. Neumann P., Pozárková D., Vrána J., Dolezel J., Macas J. Chromosome sorting and PCR-based physical mapping in pea (Pisum sativum L.). Chromosome Res. 2002;10:63-71.

111. Nogler G.A. The lesser-known Mendel: his experiments on Hieracium. Genetics. 2006;172:1-6.

112. Novák P., Neumann P., Macas J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics. 2010;11:378. DOI: 10.1186/14712105-11-378

113. Pellew C., Sansome E.R. Genetical and cytological studies on the relation between Asiatic and European varieties of Pisum sativum. I. Partial Sterility in hybrids of a Thibetian and a European variety (by C. Pellew). II. Chromosome association in Pisum (by E.R. Sansome). J. Genet. 1932;25:25-54.

114. Rameau D., Dénoue D., Fraval F., Haurogné H., Josserand J., Lacuou L., Batge S., Murfet I.C. Genetic mapping in pea. 2. Identification of RAPD and SCAR markers linked to genes affecting plant architecture. Theor. Appl. Genet. 1998;97:916-928.

115. Saalbach G., Erik P., Wienkoop S. Characterisation by proteomics of peribacteroid space and peribacteroid membrane preparations from pea (Pisum sativum) symbiosomes. Proteomics. 2002;2: 325-337.

116. Sansome E.R. Segmental interchange in Pisum sativum. Cytologia. 1932;2:200-219.

117. Sansome E.R. Segmental interchange in Pisum sativum. II. Cytologia. 1933;5:15-30.

118. Sansome E.R. Segmental interchange lines in Pisum sativum. Nature. 1938;142:674-675.

119. Sasaki Y., Nagano Y. Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci. Biotechnol. Biochem. 2004;68:1175-1184.

120. Schiltz S., Gallardo K., Huart M., Negroni L., Sommerer N., Burstin J. Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol. 2004;135:2241-2260.

121. Smýkal P., Aubert G., Burstin J., Coyne C.J., Ellis N.T., Flavell A.J., Ford R., Hýbl M., Macas I., Neumann P., McPhee K.E., Redden R.J., Rubiales D., Weller J.L., Warkentin T.D. Pea (Pisum sativum L.) in the genomic era. Agronomy. 2012;2:74-115.

122. Snoad B. A preliminary assessment of ‘leafless peas’. Euphytica. 1974;23:257-265.

123. Somers D.A., Samac D.A., Olhoft P.M. Recent advances in legume transformation. Plant Physiol. 2003;131:892-899.

124. Svabova L., Smýkal P., Griga M., Ondrej V. Agrobacterium-mediated transformation of Pisum sativum in vitro and in vivo. Biol. Plant. 2005;49:361-370.

125. Tattersall A.D., Turner L., Knox M.R., Ambrose M.J., Ellis T.H.N., Hofer J.M.I. The mutant crispa reveals multiple roles for PHANTASTICA in pea compound leaf development. Plant Cell. 2005;17:1046-1060.

126. Temnykh S.V., Weeden N.F. A brief synopsis of the current status of pea cytogenetics. Pisum Genet. 1993;25:1-4.

127. The International Aphid Genomics Consortium. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 2010;8:e1000313. DOI: 10.1371/journal.pbio.1000313

128. Trusov Y.A., Bogdanova V.S., Berdnikov V.A. Evolution of regular zone of histone H1 in Fabaceae plants. J. Mol. Evol. 2004;59: 546-555.

129. Vershinin A.V., Allnutt T.R., Knox M.R., Ambrose M.J. Transposable elements reveal the impact of introgression, rather than transposition, in Pisum diversity, evolution, and domestication. Mol. Biol. Evol. 2003;20:2067-2075.

130. Weeden N.F., Boone W.E. Mapping the Rb locus on linkage group III using long PCR followed by endonuclease digestion. Pisum Genet. 1999;31:36.

131. Weeden N.F., Ellis T.H.N., Timmerman-Vaughan G.M., Swiecicki W.K., Rozov S.M., Berdnikov V.A. A consensus linkage map for Pisum sativum. Pisum Genet. 1998;30:1-3.

132. Weeden N.F., Marx G. Further genetic analysis and linkage relationships of isozyme loci in the pea: Confirmation of the diploid nature of the genome. J. Hered. 1987;78:153-159.

133. Wellensiek S.J. Genetic monograph on Pisum. Bibliographia Genetica.1925;2:343-476.

134. Zaytseva O.O., Bogdanova V.S., Kosterin O.E. Phylogenetic reconstruction at the species and intraspecies levels in the genus Pisum (L.) (peas) using a histone H1 gene. Gene. 2012;504:192-202.

135. Zaytseva O.O., Gunbin K.V., Mglinets A.V., Kosterin O.E. Divergence and population traits in evolution of the genus Pisum L. as reconstructed using genes of two histone H1 subtypes showing different phylogenetic resolution. Gene. 2015;556:235-244.

136. Zhu C., Gore M., Buckler E.S., Yu J. Status and prospects of association mapping in plants. Plant Genome. 2008;1:5-20.

This entry was posted in Tom 19-1. Bookmark the permalink.