Application of Quantitative Trait Loci (QTL) mapping to study the interactions of pea (Pisum sativum L.) with rhizosphere microorganisms
- Authors: Zhernakov A.I.1, Gordon M.L.1,2, Zorin E.A.1, Sulima A.S.1, Zhukov V.A.1,2
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Affiliations:
- All-Russia Research Institute for Agricultural Microbiology
- N.I. Vavilov All-Russian Institute of Plant Genetic Resources
- Issue: Vol 23, No 1 (2025)
- Pages: 65-79
- Section: Methodology in ecological genetics
- Submitted: 09.12.2024
- Accepted: 13.12.2024
- Published: 19.04.2025
- URL: https://journals.eco-vector.com/ecolgenet/article/view/642710
- DOI: https://doi.org/10.17816/ecogen642710
- ID: 642710
Cite item
Abstract
The review is devoted to the application of quantitative trait loci (QTL) analysis to study the interactions of common pea (Pisum sativum L.), one of the most important grain legumes, with soil microorganisms. Pea, like other legumes, forms symbioses with nodule bacteria and arbuscular mycorrhiza fungi. The formation of symbioses leads to improved nitrogen and phosphorus nutrition of plants, resulting in increased plant resistance to abiotic and biotic stress factors, in particular, to phytopathogens. The main objective of QTL analysis is to identify genomic regions whose allelic state affects the manifestation of quantitative traits, including such traits as nitrogen fixation efficiency and pathogen resistance. The identified QTLs and molecular markers created on their basis can be used in the selection of new pea varieties with improved agronomic characteristics, such as resistance to changing environmental conditions and high efficiency of symbiotic systems. This article reviews the historical stages of the emergence of QTL analysis, the basic principles of QTL mapping, and modern approaches. The need for an integrated approach to the analysis of the characteristics of symbiosis efficiency and stability is noted, and the use of integrated phenotypic assessments for working with such traits is discussed.
Keywords
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About the authors
Aleksandr I. Zhernakov
All-Russia Research Institute for Agricultural Microbiology
Author for correspondence.
Email: azhernakov@arriam.ru
ORCID iD: 0000-0001-8961-9317
Russian Federation, Saint Petersburg
Mikhail L. Gordon
All-Russia Research Institute for Agricultural Microbiology; N.I. Vavilov All-Russian Institute of Plant Genetic Resources
Email: m.gordon.zelenoborsky@gmail.com
ORCID iD: 0000-0001-9637-9059
SPIN-code: 6385-2305
Russian Federation, Saint Petersburg; Saint Petersburg
Evgeny A. Zorin
All-Russia Research Institute for Agricultural Microbiology
Email: ezorin@arriam.ru
ORCID iD: 0000-0001-5666-3020
SPIN-code: 5048-0203
Cand. Sci. (Biology)
Russian Federation, Saint PetersburgAnton S. Sulima
All-Russia Research Institute for Agricultural Microbiology
Email: asulima@arriam.ru
ORCID iD: 0000-0002-2300-857X
SPIN-code: 4906-1159
Cand. Sci. (Biology)
Russian Federation, Saint PetersburgVladimir A. Zhukov
All-Russia Research Institute for Agricultural Microbiology; N.I. Vavilov All-Russian Institute of Plant Genetic Resources
Email: vzhukov@arriam.ru
ORCID iD: 0000-0002-2411-9191
SPIN-code: 2610-3670
Cand. Sci. (Biology)
Russian Federation, Saint Petersburg; Saint PetersburgReferences
- Wallace JG, Rodgers-Melnick E, Buckler ES. On the road to breeding 4.0: unraveling the good, the bad, and the boring of crop quantitative genomics. Annu Rev Genet. 2018;52(1):421–444. doi: 10.1146/annurev-genet-120116-024846
- Paran I, Zamir D. Quantitative traits in plants: beyond the QTL. Trends Genet. 2003;19(6):303–306. doi: 10.1016/S0168-9525(03)00117-3
- Liu Y, Zhu B, Tang J, et al. Epistatic interaction has the reverse effects with its constitutive quantitative trait loci. Sci Rep. 2024;14(1):18169. doi: 10.1038/s41598-024-69236-3
- Hasan N, Choudhary S, Naaz N, et al. Recent advancements in molecular marker-assisted selection and applications in plant breeding programmes. J Genet Eng Biotechnol. 2021;19(1):128. doi: 10.1186/s43141-021-00231-1
- Bastianelli D, Grosjean F, Peyronnet C, et al. Feeding value of pea (Pisum sativum L.) 1. Chemical composition of different categories of pea. Anim Sci. 1998;67(3):609–619. doi: 10.1017/S1357729800033051
- Dahl WJ, Foster LM, Tyler RT. Review of the health benefits of peas (Pisum sativum L.). Br J Nutr. 2012;108(S1):S3–S10. doi: 10.1017/S0007114512000852
- Shanthakumar P, Klepacka J, Bains A, et al. The current situation of pea protein and its application in the food industry. Molecules. 2022;27(16):5354. doi: 10.3390/molecules27165354
- Smýkal P, Aubert G, Burstin J, et al. Pea (Pisum sativum L.) in the genomic era. Agronomy. 2012;2(2):74–115. doi: 10.3390/agronomy2020074
- Dowarah B, Gill SS, Agarwala N. Arbuscular mycorrhizal fungi in conferring tolerance to biotic stresses in plants. J Plant Growth Regul. 2022;41(4):1429–1444. doi: 10.1007/s00344-021-10392-5
- Leppyanen IV, Shakhnazarova VY, Shtark OY, et al. Receptor-like kinase LYK9 in Pisum sativum L. Is the CERK1-Like receptor that controls both plant immunity and AM symbiosis development. Int J Mol Sci. 2017;19(1):8. doi: 10.3390/ijms19010008
- Jha AB, Gali KK, Alam Z, et al. Potential application of genomic technologies in breeding for fungal and oomycete disease resistance in pea. Agronomy. 2021;11(6):1260. doi: 10.3390/agronomy11061260
- Goyal RK, Mattoo AK, Schmidt MA. Rhizobial-host interactions and symbiotic nitrogen fixation in legume crops toward agriculture sustainability. Front Microbiol. 2021;12:669404. doi: 10.3389/fmicb.2021.669404
- Kreplak J, Madoui M-A, Cápal P, et al. A reference genome for pea provides insight into legume genome evolution. Nat Genet. 2019;51(9):1411–1422. doi: 10.1038/s41588-019-0480-1
- Shan Y. Beyond Mendelism and biometry. Stud Hist Philos Sci A. 2021;89:155–163. doi: 10.1016/j.shpsa.2021.08.014
- Barton NH, Etheridge AM, Véber A. The infinitesimal model: Definition, derivation, and implications. Theor Popul Biol. 2017;118:50–73. doi: 10.1016/j.tpb.2017.06.001
- Thoday JM. Location of polygenes. Nature. 1961;191(4786): 368–370. doi: 10.1038/191368a0
- Weeden NF, Muehlbauer FJ, Ladizinsky G. Extensive conservation of linkage relationships between pea and lentil genetic maps. J Hered. 1992;83(2):123–129. doi: 10.1093/oxfordjournals.jhered.a111171
- Lockhart DJ, Dong H, Byrne MC, et al. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat Biotechnol. 1996;14(13):1675–1680. doi: 10.1038/nbt1296-1675
- Dmitriev AA, Pushkova EN, Melnikova NV. Plant genome sequencing: modern technologies and novel opportunities for breeding. Molecular Biology. 2022;54(4):531–545. doi: 10.31857/S0026898422040048 EDN: NKLZQP
- Clauw P, Ellis TJ, Liu H-J, Sasaki E. Beyond the standard GWAS — A guide for plant biologists. Plant Cell Physiol. 2024; pcae079. doi: 10.1093/pcp/pcae079
- Zhang Y, Wang M, Li Z, et al. An overview of detecting gene-trait associations by integrating GWAS summary statistics and eQTLs. Sci China Life Sci. 2024;67(6):1133–1154. doi: 10.1007/s11427-023-2522-8
- Abiola O, Angel JM, Avner P, et al. The nature and identification of quantitative trait loci: a community’s view. Nat Rev Genet. 2003;4(11):911–916. doi: 10.1038/nrg1206
- Kao C-H. Mapping quantitative trait loci using the experimental designs of recombinant inbred populations. Genetics. 2006;174(3):1373–1386. doi: 10.1534/genetics.106.056416
- Keurentjes JJB, Bentsink L, Alonso-Blanco C, et al. Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics. 2007;175(2):891–905. doi: 10.1534/genetics.106.066423
- Tanksley SD, Nelson JC. Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theor Appl Genet. 1996;92(2):191–203. doi: 10.1007/BF00223376
- Filiault DL, Seymour DK, Maruthachalam R, Maloof JN. The generation of doubled haploid lines for QTL mapping. In: Busch W, editor. Plant genomics. Methods in molecular biology. Vol. 1610. New York: Humana Press; 2017. P. 39–57. doi: 10.1007/978-1-4939-7003-2_4
- Cavanagh C, Morell M, Mackay I, Powell W. From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr Opin Plant Biol. 2008;11(2):215–221. doi: 10.1016/j.pbi.2008.01.002
- Yu J, Holland JB, McMullen MD, Buckler ES. Genetic design and statistical power of nested association mapping in maize. Genetics. 2008;178(1):539–551. doi: 10.1534/genetics.107.074245
- Amiteye S. Basic concepts and methodologies of DNA marker systems in plant molecular breeding. Heliyon. 2021;7(10):e08093. doi: 10.1016/j.heliyon.2021.e08093
- Tayeh N, Aluome C, Falque M, et al. Development of two major resources for pea genomics: the GenoPea 13.2K SNP Array and a high-density, high-resolution consensus genetic map. Plant J. 2015;84(6):1257–1273. doi: 10.1111/tpj.13070
- Elshire RJ, Glaubitz JC, Sun Q, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6(5):e19379. doi: 10.1371/journal.pone.0019379
- Miller MR, Dunham JP, Amores A, et al. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res. 2007;17(2):240–248. doi: 10.1101/gr.5681207
- Duarte J, Rivière N, Baranger A, et al. Transcriptome sequencing for high throughput SNP development and genetic mapping in Pea. BMC Genom. 2014;15(1):126. doi: 10.1186/1471-2164-15-126
- Zhernakov AI, Shtark OY, Kulaeva OA, et al. Mapping-by-sequencing using NGS-based 3’-MACE-Seq reveals a new mutant allele of the essential nodulation gene Sym33 (IPD3) in pea (Pisum sativum L.). PeerJ. 2019;7: e6662. doi: 10.7717/peerj.6662
- Zawada AM, Rogacev KS, Müller S, et al. Massive analysis of cDNA Ends (MACE) and miRNA expression profiling identifies proatherogenic pathways in chronic kidney disease. Epigenetics. 2014;9(1):161–172. doi: 10.4161/epi.26931
- Michelmore RW, Paran I, Kesseli RV. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. PNAS USA. 1991;88(21):9828–9832. doi: 10.1073/pnas.88.21.9828
- Zheng Y, Xu F, Li Q, et al. QTL mapping combined with bulked segregant analysis identify SNP markers linked to leaf shape traits in Pisum sativum using SLAF sequencing. Front Genet. 2018;9:615. doi: 10.3389/fgene.2018.00615
- Zhao C, Zhang Y, Du J, et al. Crop phenomics: Current status and perspectives. Front Plant Sci. 2019;10:714. doi: 10.3389/fpls.2019.00714
- Klein A, Houtin H, Rond C, et al. QTL analysis of frost damage in pea suggests different mechanisms involved in frost tolerance. Theor Appl Genet. 2014;127(6):1319–1330. doi: 10.1007/s00122-014-2299-6
- Lavaud C, Baviere M, Le Roy G, et al. Single and multiple resistance QTL delay symptom appearance and slow down root colonization by Aphanomyces euteiches in pea near isogenic lines. BMC Plant Biol. 2016;16(1):166. doi: 10.1186/s12870-016-0822-4
- Bourion V, Rizvi SMH, Fournier S, et al. Genetic dissection of nitrogen nutrition in pea through a QTL approach of root, nodule, and shoot variability. Theor Appl Genet. 2010;121(1):71–86. doi: 10.1007/s00122-010-1292-y
- Kaeppler SM, Parke JL, Mueller SM, et al. Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci. 2000;40(2):358–364. doi: 10.2135/cropsci2000.402358x
- Shtark OY, Zhernakov AI, Kichigina NE, et al. Effect of mutations in the Sym7, Sym19 and Sym34 genes on the interaction of pea (Pisum sativum L.) with the arbuscular mycorrhizal fungus Rhizophagus irregularis. Ecological genetics. 2024;22(3):225–242. doi: 10.17816/ecogen624607 EDN: NAIZZI
- Zheng G, Yuan A, Li Q, Gastwirth JL. Single marker association analysis for unrelated samples. In: Elston R, editor. Statistical human genetics. Methods in molecular biology. Vol. 1666. New York: Humana Press; 2017. P. 375–389. doi: 10.1007/978-1-4939-7274-6_18
- Lander ES, Botstein D. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics. 1989;121(1):185–199. doi: 10.1093/genetics/121.1.185
- Jansen RC, Stam P. High resolution of quantitative traits into multiple loci via interval mapping. Genetics. 1994;136(4):1447–1455. doi: 10.1093/genetics/136.4.1447
- Kao C-H, Zeng Z-B, Teasdale RD. Multiple interval mapping for quantitative trait loci. Genetics. 1999;152(3):1203–1216. doi: 10.1093/genetics/152.3.1203
- Kulaeva OA, Zhernakov AI, Afonin AM, et al. Pea marker database (PMD) — a new online database combining known pea (Pisum sativum L.) gene-based markers. PLoS ONE. 2017;12(10):e0186713. doi: 10.1371/journal.pone.0186713
- Dirlewanger E, Isaac PG, Ranade S, et al. Restriction fragment length polymorphism analysis of loci associated with disease resistance genes and developmental traits in Pisum sativum L. Theoret Appl Genetics. 1994;88(1):17–27. doi: 10.1007/BF00222388
- Van Der Plank JE. Disease resistance in plants. New York: Academic Press; 1968. 206 p.
- Sulima AS, Zhukov VA. War and peas: Molecular bases of resistance to powdery mildew in pea (Pisum sativum L.) and other legumes. Plants. 2022;11(3):339. doi: 10.3390/plants11030339
- Timmerman-Vaughan GM, Moya L, Frew TJ, et al. Ascochyta blight disease of pea (Pisum sativum L.): defence-related candidate genes associated with QTL regions and identification of epistatic QTL. Theor Appl Genet. 2016;129(5):879–896. doi: 10.1007/s00122-016-2669-3
- Jha AB, Gali KK, Tar’an B, Warkentin TD. Fine mapping of QTLs for ascochyta blight resistance in pea using heterogeneous inbred families. Front Plant Sci. 2017;8:765. doi: 10.3389/fpls.2017.00765
- Timmerman-Vaughan GM, Frew TJ, Butler R, et al. Validation of quantitative trait loci for Ascochyta blight resistance in pea (Pisum sativum L.), using populations from two crosses. Theor Appl Genet. 2004;109(8):1620–1631. doi: 10.1007/s00122-004-1779-5
- Wu L, Fredua-Agyeman R, Hwang S-F, et al. Mapping QTL associated with partial resistance to Aphanomyces root rot in pea (Pisum sativum L.) using a 13.2 K SNP array and SSR markers. Theor Appl Genet. 2021;134(9):2965–2990. doi: 10.1007/s00122-021-03871-6
- Wu L, Fredua-Agyeman R, Strelkov SE, et al. Identification of quantitative trait loci associated with partial resistance to fusarium root rot and wilt caused by fusarium graminearum in field pea. Front Plant Sci. 2021;12:784593. doi: 10.3389/fpls.2021.784593
- Coyne CJ, Porter LD, Boutet G, et al. Confirmation of Fusarium root rot resistance QTL Fsp-Ps 2.1 of pea under controlled conditions. BMC Plant Biol. 2019;19(1):98. doi: 10.1186/s12870-019-1699-9
- Rai R, Singh AK, Singh BD, et al. Molecular mapping for resistance to pea rust caused by Uromyces fabae (Pers.) de-Bary. Theor Appl Genet. 2011;123(5):803–813. doi: 10.1007/s00122-011-1628-2
- Ashtari Mahini R, Kumar A, Elias EM, et al. Analysis and identification of QTL for resistance to Sclerotinia sclerotiorum in pea (Pisum sativum L.). Front Genet. 2020;11:587968. doi: 10.3389/fgene.2020.587968
- Zhukov VA, Akhtemova GA, Zhernakov AI, et al. Evaluation of the symbiotic effectiveness of pea (Pisum sativum L.) genotypes in pot experiment. Agricultural Biology. 2017;52(3):607–614. doi: 10.15389/agrobiology.2017.3.607rus EDN: YZKVLX
- Zhukov VA, Zhernakov AI, Sulima AS, et al. Association study of symbiotic genes in pea (Pisum sativum L.) cultivars grown in symbiotic conditions. Agronomy. 2021;11(11):2368. doi: 10.3390/agronomy11112368
- Li D, Kinkema M, Gresshoff PM. Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation. J Plant Physiol. 2009;166(9):955–967. doi: 10.1016/j.jplph.2009.03.004
- Zipfel C, Oldroyd GED. Plant signalling in symbiosis and immunity. Nature. 2017;543(7645):328–336. doi: 10.1038/nature22009
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