Genetic variability assessment of 127 Triticum turgidum L. accessions for mycorrhizal susceptibility-related traits detection.
Fungi
/ physiology
Genes, Plant
Genetic Variation
Genome-Wide Association Study
Mycorrhizae
/ physiology
Phylogeny
Plant Breeding
Plant Roots
/ microbiology
Plant Shoots
/ growth & development
Polymorphism, Single Nucleotide
Quantitative Trait Loci
Symbiosis
/ genetics
Tetraploidy
Triticum
/ genetics
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
28 06 2021
28 06 2021
Historique:
received:
05
03
2021
accepted:
02
06
2021
entrez:
29
6
2021
pubmed:
30
6
2021
medline:
9
11
2021
Statut:
epublish
Résumé
Positive effects of arbuscular mycorrhizal fungi (AMF)-wheat plant symbiosis have been well discussed by research, while the actual role of the single wheat genotype in establishing this type of association is still poorly investigated. In this work, the genetic diversity of Triticum turgidum wheats was exploited to detect roots susceptibility to AMF and to identify genetic markers in linkage with chromosome regions involved in this symbiosis. A tetraploid wheat collection of 127 accessions was genotyped using 35K single-nucleotide polymorphism (SNP) array and inoculated with the AMF species Funneliformis mosseae (F. mosseae) and Rhizoglomus irregulare (R. irregulare), and a genome-wide association study (GWAS) was conducted. Six clusters of genetically related accessions were identified, showing a different mycorrhizal colonization among them. GWAS revealed four significant quantitative trait nucleotides (QTNs) involved in mycorrhizal symbiosis, located on chromosomes 1A, 2A, 2B and 6A. The results of this work enrich future breeding activities aimed at developing new grains on the basis of genetic diversity on low or high susceptibility to mycorrhization, and, possibly, maximizing the symbiotic effects.
Identifiants
pubmed: 34183734
doi: 10.1038/s41598-021-92837-1
pii: 10.1038/s41598-021-92837-1
pmc: PMC8239029
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13426Références
Feldlichman, M. & Kislev, M. E. Domestication of emmer wheat and evolution of free-threshing tetraploid wheat. Israel J. Plant Sci. 55(3–4), 207–221 (2007).
doi: 10.1560/IJPS.55.3-4.207
Martínez-Moreno, F. et al. Durum wheat in the Mediterranean Rim: Historical evolution and genetic resources. Genet. Resour. Crop Evol. 1–22 (2020).
Alvaro, F., Isidro, J., Villegas, D., Garcia del Moral, L. F. & Royo, C. Old and modern durum wheat varieties from Italy and Spain differ in main spike components. Field Crops Res. 106, 86–93 (2008).
doi: 10.1016/j.fcr.2007.11.003
Fu, Y. & Somers, D. J. Genome-wide reduction of genetic diversity in wheat breeding. Crop Sci. 49, 161–168 (2009).
doi: 10.2135/cropsci2008.03.0125
Fu, Y. B. Understanding crop genetic diversity under modern plant breeding. Theor. Appl. Genet. 128, 2131–2142 (2015).
pubmed: 26246331
pmcid: 4624815
doi: 10.1007/s00122-015-2585-y
Lichtfouse, E. Sustainable agriculture as a central science to solve global society issues. In Organic Farming, Pest Control and Remediation of Soil Pollutants (ed. Lichtfouse, E.) 1–3 (Holland, 2009).
Nazco, R. et al. Can Mediterranean durum wheat landraces contribute to improved grain quality attributes in modern cultivars?. Euphytica 185, 1–17 (2012).
doi: 10.1007/s10681-011-0588-6
Taranto, F. et al. Whole genome scan reveals molecular signatures of divergence and selection related to important traits in durum wheat germplasm. Front. Genet. 11, 217 (2020).
pubmed: 32373150
doi: 10.3389/fgene.2020.00217
Chaparro, J. M., Sheflin, A. M., Manter, D. K. & Vivanco, J. M. Manipulating the soil microbiome to increase soil health and plant fertility. Biol. Fertil. Soils 48(5), 489–499 (2012).
doi: 10.1007/s00374-012-0691-4
Thirkell, T. J., Charters, M. D., Elliott, A. J., Sait, S. M. & Field, K. J. Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J. Ecol. 105, 921–929 (2017).
doi: 10.1111/1365-2745.12788
Stürmer, S. L., Bever, J. D. & Morton, J. B. Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): A phylogenetic perspective on species distribution patterns. Mycorrhiza 28(7), 587–603 (2018).
pubmed: 30187122
doi: 10.1007/s00572-018-0864-6
Brundrett, M. C. Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320(1–2), 37–77 (2009).
doi: 10.1007/s11104-008-9877-9
Wipf, D., Krajinski, F., van Tuinen, D., Recorbet, G. & Courty, P. Trading on the arbuscular mycorrhiza market: From arbuscules to common mycorrhizal networks. New Phytol. 223, 1127–1142 (2019).
pubmed: 30843207
doi: 10.1111/nph.15775
Evelin, H., Giri, B. & Kapoor, R. Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed, Trigonella foenum-graecum. Mycorrhiza 22, 203–217 (2012).
pubmed: 21695577
doi: 10.1007/s00572-011-0392-0
Symanczik, S., Lehmann, M. F., Wiemken, A., Boller, T. & Courty, P. E. Effects of two contrasted arbuscular mycorrhizal fungal isolates on nutrient uptake by Sorghum bicolor under drought. Mycorrhiza 28, 779–785 (2018).
pubmed: 30006910
doi: 10.1007/s00572-018-0853-9
Sawers, R. J., Gutjahr, C. & Paszkowski, U. Cereal mycorrhiza: An ancient symbiosis in modern agriculture. Trends Plant Sci. 13, 93–97 (2008).
pubmed: 18262822
doi: 10.1016/j.tplants.2007.11.006
Lehmann, A., Barto, E. K., Powell, J. R. & Rillig, M. C. Mycorrhizal responsiveness trends in annual crop plants and their wild relatives—A meta-analysis on studies from 1981 to 2010. Plant Soil 355, 231–250 (2012).
doi: 10.1007/s11104-011-1095-1
Ryan, M. H. & Graham, J. H. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol. 220, 1092–1107 (2018).
pubmed: 29987890
doi: 10.1111/nph.15308
Lehnert, H., Serfling, A., Enders, M., Friedt, W. & Ordon, F. Genetics of mycorrhizal symbiosis in winter wheat (Triticum aestivum). New Phytol. 215, 779–791 (2017).
pubmed: 28517039
doi: 10.1111/nph.14595
Davidson, H. et al. Spatial effects and GWA mapping of root colonization assessed in the interaction between the rice diversity panel 1 and an arbuscular mycorrhizal fungus. Front. Plant Sci. 10, 633 (2019).
pubmed: 31156686
pmcid: 6533530
doi: 10.3389/fpls.2019.00633
Plouznikoff, K., Asins, M. J., de Boulois, H. D., Carbonell, E. A. & Declerck, S. Genetic analysis of tomato root colonization by arbuscular mycorrhizal fungi. Ann. Bot. 124, 933–946 (2019).
pubmed: 30753410
pmcid: 7145532
Leiser, W. L. et al. No need to breed for enhanced colonization by arbuscular mycorrhizal fungi to improve low-P adaptation of West African sorghums. Plant Soil 401, 51–64 (2016).
doi: 10.1007/s11104-015-2437-1
Turrini, A. et al. Large variation in mycorrhizal colonization among wild accessions, cultivars, and inbreds of sunflower (Helianthus annuus L.). Euphytica 207, 331–342 (2016).
doi: 10.1007/s10681-015-1546-5
Aranzana, M. J. et al. Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet. 1(5), e60 (2005).
pubmed: 16292355
pmcid: 1283159
doi: 10.1371/journal.pgen.0010060
Thoen, M. P. et al. Genetic architecture of plant stress resistance: Multi-trait genome-wide association mapping. New Phytol. 213(3), 1346–1362 (2017).
pubmed: 27699793
doi: 10.1111/nph.14220
Quero, G. et al. Genome-wide association study using historical breeding populations discovers genomic regions involved in high-quality rice. Plant Genome 11(3), 1–12 (2018).
doi: 10.3835/plantgenome2017.08.0076
Tao, Y. et al. Whole genome scan reveals molecular signatures of divergence and selection related to important traits in durum wheat germplasm. Front. Genet. 11, 217 (2020).
doi: 10.3389/fgene.2020.00217
Kumar, N., Kulwal, P. L. & Balyan, H. S. QTL mapping for yield and yield contributing traits in two mapping populations of bread wheat. Mol. Breed. 19, 163–177 (2007).
doi: 10.1007/s11032-006-9056-8
Li, S. et al. A intervarietal genetic map and QTL analysis for yield traits in wheat. Mol. Breed. 20, 167–178 (2007).
doi: 10.1007/s11032-007-9080-3
Jiang, P. et al. A novel QTL on chromosome 5AL of Yangmai 158 increases resistance to Fusarium head blight in wheat. Plant Pathol. 69, 249–258 (2020).
doi: 10.1111/ppa.13130
Ollier, M. et al. QTL mapping and successful introgression of the spring wheat-derived QTL Fhb1 for Fusarium head blight resistance in three European triticale populations. Theor. Appl. Genet. 133, 457–477 (2020).
pubmed: 31960090
doi: 10.1007/s00122-019-03476-0
Hetrick, B., Wilson, G. W. T., Gill, B. & Cox, T. Chromosome location of mycorrhizal responsive genes in wheat. Can. J. Bot. 73(6), 891–897 (1995).
doi: 10.1139/b95-097
Singh, A. K., Hamel, C., DePauw, R. M. & Knox, R. E. Genetic variability in arbuscular mycorrhizal fungi compatibility supports the selection of durum wheat genotypes for enhancing soil ecological services and cropping systems in Canada. Can. J. Microbiol. 58, 293–302 (2012).
pubmed: 22356605
doi: 10.1139/w11-140
Ellouze, W. et al. Potential to breed for mycorrhizal association in durum wheat. Can. J. Microbiol. 62, 263–271 (2016).
pubmed: 26825726
doi: 10.1139/cjm-2014-0598
De Vita, P. et al. Genetic markers associated to arbuscular mycorrhizal colonization in durum wheat. Sci. Rep. 8, 1–12 (2018).
Kronstad, W. E. Agricultural development and wheat breeding in the 20th century. In Wheat: Prospects for Global Improvement. Developments in Plant Breeding (eds Braun, H. J. et al.) (Springer, 1997).
Waines, J. G. & Ehdaie, B. Domestication and crop physiology: Roots of green-revolution wheat. Ann. Bot. 100(5), 991–998 (2007).
pubmed: 17940075
doi: 10.1093/aob/mcm180
Barcaccia, G., Molinari, L., Porfiri, O. & Veronesi, F. Molecular characterization of emmer (Triticum dicoccon Schrank) Italian landraces. Genet. Resour. Crop. Evol. 49, 417–428 (2002).
doi: 10.1023/A:1020650804532
Chandrasekhar, K., Nashef, K. & Ben-David, R. Agronomic and genetic characterization of wild emmer wheat (Triticum turgidum subsp. dicoccoides) introgression lines in a bread wheat genetic background. Genet. Resour. Crop. Evol. 64, 1917–1926 (2017).
doi: 10.1007/s10722-016-0481-1
De Cillis, U. Syntax of referencing in I frumenti Siciliani. Stazione sperimentale di granicoltura per la Sicilia (ed. Maiomone, G.) 1–323 (Italy, 1942).
Pawlowski, M. L., Vuong, T. D., Valliyodan, B., Nguyen, H. T. & Hartman, G. L. Whole-genome resequencing identifies quantitative trait loci associated with mycorrhizal colonization of soybean. Theor. Appl. Genet. 133, 409–417 (2020).
pubmed: 31707439
doi: 10.1007/s00122-019-03471-5
Zhu, Y. G., Smith, S. E., Barrit, A. R. & Smith, F. A. Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237, 249–255 (2001).
doi: 10.1023/A:1013343811110
Mustafa, G. et al. Phosphorus supply, arbuscular mycorrhizal fungal species, and plant genotype impact on the protective efficacy of mycorrhizal inoculation against wheat powdery mildew. Mycorrhiza 26, 685–697 (2016).
pubmed: 27130314
doi: 10.1007/s00572-016-0698-z
Hayman, D. Plant growth responses to vesicular-arbuscular mycorrhiza vi. Effect of light and temperature. New Phytol. 73, 71–80 (1974).
doi: 10.1111/j.1469-8137.1974.tb04607.x
Daft, M. & El-Giahmi, A. Effect of arbuscular mycorrhiza on plant growth: viii. Effects of defoliation and light on selected hosts. New Phytol. 80, 365–372 (1978).
doi: 10.1111/j.1469-8137.1978.tb01570.x
Hetrick, B. A. D. & Bloom, J. The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. Mycologia 76, 953–956 (1984).
doi: 10.1080/00275514.1984.12023937
Gavito, M. E. et al. Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi. New Phytol. 168, 179–188 (2005).
pubmed: 16159332
doi: 10.1111/j.1469-8137.2005.01481.x
Mosse, B., Hayman, D. S. & Arnold, D. J. Plant growth responses to vesicular-arbuscular mycorrhizal. V. Phosphate uptake by three plant species from P-deficient soils labeled with 32p. New Phytol. 72, 809–815 (1973).
doi: 10.1111/j.1469-8137.1973.tb02056.x
Azcon, R. & Ocampo, J. A. Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytol. 87, 677–685 (1981).
doi: 10.1111/j.1469-8137.1981.tb01702.x
Dreyer, B., Honrubia, M. & Morte, A. How root structure defines the arbuscular mycorrhizal symbiosis and what we can learn from it? In Root Engineering. Soil Biology (eds Morte, A. & Varma, A.) 40 (Springer, 2014).
Eissenstat, D. M., Kucharski, J. M., Zadworny, M., Adams, T. S. & Koide, R. T. Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol. 208, 114–124 (2015).
pubmed: 25970701
doi: 10.1111/nph.13451
Baudoin, E., Benizri, E. & Guckert, A. Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol. Biochem. 35, 1183–1192 (2003).
doi: 10.1016/S0038-0717(03)00179-2
Yao, Q., Wang, L. R., Zhu, H. H. & Chen, J. Z. Effects of arbuscular mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Sci. Hortic. 121, 458–461 (2009).
doi: 10.1016/j.scienta.2009.03.013
Chen, W. et al. Arbuscular mycorrhizal fungus enhances lateral root formation in Poncirus trifoliata (L.) as revealed by RNA-Seq analysis. Front. Plant Sci. 8, 2039 (2017).
pubmed: 29238356
doi: 10.3389/fpls.2017.02039
Lucini, L. et al. Inoculation of Rhizoglomus irregulare or Trichoderma atroviride differentially modulates metabolite profiling of wheat root exudates. Phytochemistry 157, 158–167 (2019).
pubmed: 30408729
doi: 10.1016/j.phytochem.2018.10.033
Veresoglou, S. D., Menexes, G. & Rillig, M. C. Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22, 227–235 (2012).
pubmed: 21710352
doi: 10.1007/s00572-011-0398-7
Sedgwick, P. Multiple significance tests: The Bonferroni correction. Bmj. 344 (2012).
Klingner, A., Hundeshagen, B., Kernebeck, H. & Bothe, H. Localization of the yellow pigment formed in roots of gramineous plants colonized by arbuscular fungi. Protoplasma 185, 50–57 (1995).
doi: 10.1007/BF01272753
Hassan, D. G., Zargar, M. & Beigh, G. Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microb. Ecol. 34, 74–80 (1997).
doi: 10.1007/s002489900036
Zhang, S., Lehman, A., Zheng, W., You, Z. & Rillig, M. C. Arbuscular mycorrhizal fungi increase grain yields: A meta-analysis. New Phytol. 222(1), 543–555 (2019).
pubmed: 30372522
doi: 10.1111/nph.15570
Roncallo, P. F. et al. QTL analysis of main and epistatic effects for flour color traits in durum wheat. Euphytica 185, 77–92 (2012).
doi: 10.1007/s10681-012-0628-x
Varshney, R. K. et al. Identification of eight chromosomes and a microsatellite marker on 1AS associated with QTL for grain weight in bread wheat. Theor. Appl. Genet. 100, 1290–1294 (2000).
doi: 10.1007/s001220051437
Hu, J. et al. QTL mapping for yield-related traits in wheat based on four RIL populations. Theor. Appl. Genet. 133, 917–933 (2020).
pubmed: 31897512
doi: 10.1007/s00122-019-03515-w
Mérida-García, R. et al. Mapping agronomic and quality traits in elite durum wheat lines under differing water regimes. Agronomy 10, 144 (2020).
doi: 10.3390/agronomy10010144
Zhou, W. C., Kolb, F. L., Bai, G. H., Shaner, G. E. & Domier, L. L. Genetic analysis of scab resistance QTL in wheat with microsatellite and AFLP markers. Genome 45, 719–727 (2002).
pubmed: 12175075
doi: 10.1139/g02-034
Jiang, G., Shi, J. & Ward, R. W. QTL analysis of resistance to Fusarium head blight in the novel wheat germplasm CJ 9306. I. Resistance to fungal spread. Theor. Appl. Genet. 116, 3–13 (2007).
pubmed: 17898987
doi: 10.1007/s00122-007-0641-y
Lévy, J. et al. A putative Ca2
pubmed: 14963335
doi: 10.1126/science.1093038
Liu, A. et al. Arbuscular mycorrhizae improve low temperature tolerance in cucumber via alterations in H
pubmed: 25160659
doi: 10.1007/s10265-014-0657-8
Fiorilli, V. et al. Omics approaches revealed how arbuscular mycorrhizal symbiosis enhances yield and resistance to leaf pathogen in wheat. Sci. Rep. 8(1), 1–18 (2018).
doi: 10.1038/s41598-018-27622-8
Luginbuehl, L. H. et al. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356(6343), 1175–1178 (2017).
pubmed: 28596311
doi: 10.1126/science.aan0081
Pfeffer, P. E., Douds, D. D., Becard, G. & Shachar-Hill, Y. Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 120, 587–598 (1999).
pubmed: 10364411
doi: 10.1104/pp.120.2.587
García-Garrido, J. M., García-Romera, I. & Ocampo, J. A. Cellulase production by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd) Gerd. and Trappe. New Phytol. 121, 221–226 (1992).
doi: 10.1111/j.1469-8137.1992.tb01107.x
Guether, M. et al. A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol. 150, 73–83 (2009).
pubmed: 19329566
doi: 10.1104/pp.109.136390
Kobae, Y., Tamura, Y., Takai, S., Banba, M. & Hata, S. Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol. 51, 1411–1415 (2010).
pubmed: 20627949
doi: 10.1093/pcp/pcq099
Handa, Y. et al. RNA-seq transcriptional profiling of an arbuscular mycorrhiza provides insights into regulated and coordinated gene expression in Lotus japonicus and Rhizophagus irregularis. Plant Cell Physiol. 8, 1490–1511 (2015).
doi: 10.1093/pcp/pcv071
Vangelisti, A. et al. Arbuscular mycorrhizal fungi induce the expression of specific retrotransposons in roots of sunflower (Helianthus annuus L.). PLoS ONE 14(2), e0212 (2019).
doi: 10.1371/journal.pone.0212371
Gobbato, E. Recent developments in arbuscular mycorrhizal signaling. Curr. Opin. Plant Biol. 26, 1–7 (2015).
pubmed: 26043435
doi: 10.1016/j.pbi.2015.05.006
Doyle, J. J. & Doyle, J. L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11–15 (1987).
Jombart, T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).
pubmed: 18397895
doi: 10.1093/bioinformatics/btn129
Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, 281 (2014).
doi: 10.7717/peerj.281
Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94 (2010).
pubmed: 20950446
pmcid: 2973851
doi: 10.1186/1471-2156-11-94
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30(12), 2725–2729 (2013).
pubmed: 24132122
doi: 10.1093/molbev/mst197
Paradis, E., Claude, J. & Strimmer, K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20(2), 289–290 (2004).
pubmed: 14734327
doi: 10.1093/bioinformatics/btg412
Njeru, E. M. et al. First evidence for a major cover crop effect on arbuscular mycorrhizal fungi and organic maize growth. Agron. Sustain. Dev. 34, 841–848 (2014).
doi: 10.1007/s13593-013-0197-y
Giovannetti, M. & Mosse, B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500 (1980).
doi: 10.1111/j.1469-8137.1980.tb04556.x
Hankin, R.K.S. The mvp package: fast multivariate polynomials R. R package version 1.0-5 (2020).
Liu, X., Huang, M., Fan, B., Buckler, E. S. & Zhang, Z. Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet. 10(7), e1005767 (2016).
doi: 10.1371/journal.pgen.1005767