Abstract
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We have identified QTLs for stomatal characteristics on chromosome II of faba bean by applying SNPs derived from M. truncatula , and have identified candidate genes within these QTLs using synteny between the two species.
Abstract
Faba bean (Vicia faba L.) is a valuable food and feed crop worldwide, but drought often limits its production, and its genome is large and poorly mapped. No information is available on the effects of genomic regions and genes on drought adaptation characters such as stomatal characteristics in this species, but the synteny between the sequenced model legume, Medicago truncatula, and faba bean can be used to identify candidate genes. A mapping population of 211 F5 recombinant inbred lines (Mélodie/2 × ILB 938/2) were phenotyped to identify quantitative trait loci (QTL) affecting stomatal morphology and function, along with seed weight, under well-watered conditions in a climate-controlled glasshouse in 2013 and 2014. Canopy temperature (CT) was evaluated in 2013 under water-deficit (CTd). In total, 188 polymorphic single nucleotide polymorphisms (SNPs), developed from M. truncatula genome data, were assigned to nine linkage groups that covered ~928 cM of the faba bean genome with an average inter-marker distance of 5.8 cM. 15 putative QTLs were detected, of which eight (affecting stomatal density, length and conductance and CT) co-located on chromosome II, in the vicinity of a possible candidate gene—a receptor-like protein kinase found in the syntenic interval of M. truncatula chromosome IV. A ribose-phosphate pyrophosphokinase from M. truncatula chromosome V, postulated as a possible candidate gene for the QTL for CTd, was found some distance away in the same chromosome. These results demonstrate that genomic information from M. truncatula can successfully be translated to the faba bean genome.
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References
Abdelmula AA, Link W, von Kittlitz E, Stelling S (1999) Heterosis and inheritance of drought tolerance in faba bean, Vicia faba L. Plant Breed 118:845–849
Abrash EB, Bergmann DC (2010) Regional specification of stomatal production by the putative ligand CHALLAH. Development 137:447–455
Alghamdi SS, Migdadi HM, Ammar MH, Paull JG, Siddique KHM (2012) Faba bean genomics: current status and future prospects. Euphytica 186:609–624
Arbaoui M, Link W, Satovic S, Torres AM (2008) Quantitative trait loci of frost tolerance and physiologically related trait in faba bean (Vicia faba L.). Euphytica 164:93–104
Asfaw A, Blair MW, Struik P (2012) Multienvironment quantitative trait loci analysis of photosynthate acquisition, accumulation, and remobilization traits in common bean under drought stress. Genes Genomes Genet 5:579–595
Blum A (2009) Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crops Res 112:119–123
Blum A (2011a) Plant breeding for water limited environments. Springer-Verlag, New York
Blum A (2011b) Drought resistance—is it really a complex trait? Funct Plant Biol 38:753–757
Box GEP, Cox DR (1964) An analysis of transformations. J Roy Stat Soc B 26:211–252
Boyer JS (1982) Plant productivity and environment. Science 218:443–448
Broman KW (2006) The genomes of recombinant inbred lines. Genetics 169:1133–1146
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264
Churchill G, Doerge R (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Conneally PM, Edwarks JH, Kidd KK, Lalouel J-M, Morton NE, Ott J, White R (1985) Report of the committee on methods of linkage analysis and reporting. Cytogenet Cell Genet 40:356–359
Cottage A, Gostkiewicz K, Thomas JE, Borrows R, Torres AM, O’Sullivan DM (2012a) Heterozygosity and diversity analysis using mapped SNPs in a faba bean inbreeding programme. Mol Breed 30:1799–1809
Cottage A, Webb A, Hobbs D, Khamassi K, Maalouf F, Ogbannaya F, Stoddard FL, Duc G, Link W, Thomas JE, O’Sullivan DM (2012b) SNP discovery and validation for genomic-assisted breeding of faba bean (Vicia faba L.). In: VI international conference on legume genetics and genomics (ICLGG). Hyderabad, India
Crépon K, Marget P, Peyronnet C, Carrouée B, Arese P, Duc G (2010) Nutritional value of faba bean (Vicia faba L.) seeds for feed and food. Field Crops Res 115:329–339
Cruz-Izquierdo S, Avila CM, Satovic Z, Palomino C, Gutierrez N, Ellwood SR, Phan HTT, Cubero JI, Torres AM (2012) Comparative genomics to bridge Vicia faba with model and closely-related legume species: stability of QTLs for flowering and yield-related traits. Theor Appl Genet 125:1767–1782
Cuppen E (2007) Genotyping by allele-specific amplification (KASPar). Cold Spring Harb Protoc. doi:10.1101/pdb.prot4841
Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Change 3:52–58
Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE (2012) Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Philos Trans R Soc Lond B Biol Sci 367:547–555
Duc G (1997) Faba bean (Vicia faba L.). Field Crops Res 53:99–109
Ellwood SR, Phan HTT, Jordan M, Torres AM, Avila CM, Cruz-Izquierdo S, Oliver RP (2008) Construction of a comparative genetic map in faba bean (Vicia faba L.); conservation of genome structure with Lens culinaris. BMC Genom 9:380
Erith AG (1930) The inheritance of colour, size and form of seeds, and of flower colour in Vicia faba L. Genetica 12:477–510
FAO (2012) FAOSTAT. In: Food and Agriculture Organization of the United Nations. Rome, Italy. http://faostat.fao.org/
Gailing O, Langenfeld-Hyeser R, Polle A, Finkeldey R (2008) Quantitative trait loci affecting stomatal density and growth in a Quercus robur progeny: implications for the adaptation to changing environments. Glob Chang Biol 14:1934–1946
Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T (2009) Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–1031
Henry DC (2009) Genomic, proteomic and metabolomic approaches to study drought responses in Aquilegia. Ph.D. thesis. Clemson University USA. p 123
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
Hiremath PJ, Kumar A, Penmetsa RV, Farmer A, Schlueter JA, Chamarthi SK, Whaley AM, Carrasquilla-Garcia N, Gaur PM, Upadhyaya HD, Kishor PBK, Shah TM, Cook DR, Varshney RK (2012) Large-scale development of cost-effective SNP marker assays for diversity assessment and genetic mapping in chickpea and comparative mapping in legumes. Plant Biotech J 10:716–732
Hua DP, Wang C, He J, Liao H, Duan Y, Zhu ZQ, Guo Y, Chen ZZ, Gong ZZ (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24:2546–2561
Hunt L, Gray JE (2009) The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr Biol 19:864–869
IPCC (2012) Managing the risks of extreme events and disasters to advance climate change adaptation. In: Field CB, Barros V, Stocker TF, Qin D, Dokken DG et al (eds) A special report of working groups I and II of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York, p 582
Kaur S, Pembleton LW, Cogan NOI, Savin KW, Leonforte T, Paull J, Materne M, Forster JW (2012) Transcriptome sequencing of field pea and faba bean for discovery and validation of SSR markers. BMC Genom 13:104
Kaur S, Kimber RBE, Cogan NOI, Materne M, Forster JW, Paull J (2014) SNP discovery and high-density genetic mapping in faba bean (Vicia faba L.) permits identification of QTLs for ascochyta blight resistance. Plant Sci 217–218:47–55
Khan HR, Link W, Hocking TJH, Stoddard FL (2007) Evaluation of physiological traits for improving drought tolerance in faba bean (Vicia faba L.). Plant Soil 292:205–217
Khan HR, Paull JG, Siddique KHM, Stoddard FL (2010) Faba bean breeding for drought-affected environments: a physiological and agronomic perspective. Field Crops Res 115:279–286
Khazaei H, Street K, Bari A, Mackay M, Stoddard FL (2013a) The FIGS (focused identification of germplasm strategy) approach identifies traits related to drought adaptation in Vicia faba genetic resources. PLoS One 8:e63107
Khazaei H, Street K, Santanen A, Bari A, Stoddard FL (2013b) Do faba bean (Vicia faba L.) accessions from environments with contrasting seasonal moisture availabilities differ in stomatal characteristics and related traits? Genet Resour Crop Evol 60:2343–2357
Khazaei H, O’Sullivan DM, Sillanpää MJ, Stoddard FL (2014) Genetic analysis reveals a novel locus in Vicia faba decoupling pigmentation in the flower from that in the extra-floral nectaries. Mol Breed (in press). doi:10.1007/s11032-014-0100-9
Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363
Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T, Mizuno S, Masuda Y, Irie K, Tanaka Y, Takada S, Kakimoto T, Sakagami Y (2010) Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol 51:1–8
Kosambi DD (1943) The estimation of map distance from recombination values. Ann Eugen 12:172–175
Lake JA, Woodward FI (2008) Response of stomatal numbers to CO2 and humidity: control by transpiration rate and abscisic acid. New Phytol 179:397–404
Laza MR, Kondo M, Ideta O, Barlaan E, Imbe T (2010) Quantitative trait loci for stomatal density and size in lowland rice. Euphytica 172:149–158
Liu HY, Zou GH, Liu GL, Hu SP, Li MS, Mei HW, Yu XQ, Luo LJ (2005) Correlation analysis and QTL identification for canopy temperature, leaf water potential and spikelet fertility in rice under contrasting moisture regimes. Chin Sci Bull 50:130–139
Liu Y, Subhash C, Yan J, Song C, Zhao J, Li J (2011) Maize leaf temperature responses to drought: thermal imaging and quantitative trait loci (QTL) mapping. Environ Exp Bot 71:158–165
Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage map. Mol Breed 30:1231–1235
Marshall A, Aalen RB, Audenaert D, Beeckman T, Broadley MR, Butenko MA, Caño-Delgado A, De Vries S, Dresselhaus T, Felix G, Graham NS, Foulkes J, Granier C, Greb T, Grossniklaus U, Hammond JP, Heidstra R, Hodgman C, Hothorn M, Inzé D, Østergaard L, Russinova E, Simon R, Skirycz A, Stahl Y, Zipfel C, De Smete I (2012) Tackling drought stress: receptor-like kinase presents new approaches. Plant Cell 24:2262–2278
Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870
Morris ER, Walker JC (2003) Receptor-like protein kinases: the keys to response. Curr Opin Plant Biol 6:339–342
Nadeau JA, Sack FD (2002) Control of stomatal distribution on the Arabidopsis leaf surface. Science 296:1697–1700
Osakabe Y, Mizuno S, Tanaka H, Maruyama K, Osakabe K, Todaka D, Fujita Y, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Overproduction of the membrane-bound receptor-like protein kinase 1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J Biol Chem 285:9190–9201
Ouyang SQ, Liu YF, Liu P, Lei G, He SJ, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62:316–329
Rebetzke GJ, Rattey AR, Farquhar GD, Richards RA, Condon AG (2013) Genomic regions for canopy temperature and their genetic association with stomatal conductance and grain yield in wheat. Funct Plant Biol 40:14–33
Rehman A, Malhotra R, Bett K, Tar’an B, Bueckert R, Warkentin T (2011) Mapping QTL associated with traits affecting grain yield in chickpea (Cicer arietinum L.) under terminal drought stress. Crop Sci 51:450–463
Ricciardi L (1989) Plant breeding for resistance to drought. II. Relationship between stomata and agronomic traits in Vicia faba L. genotypes. Agric Mediterr 119:424–434
Ruiz-Rodriguez MD, Avila CM, Torres AM, Fuchs J, Schubert I (2014) Anchoring of genetic linkage maps to the chromosome complement of Vicia faba L. Mol Breed 33:743–748
Sato S, Isobe S, Tabata S (2010) Structural analyses of the genomes in legumes. Curr Opin Plant Biol 13:146–152
Satovic Z, Torres AM, Cubero JI (1996) Genetic mapping of new morphological, isozyme and RAPD markers in Vicia faba L. using trisomics. Theor Appl Genet 93:1130–1138
Satovic Z, Avila CM, Cruz-Izquierdo S, Díaz-Ruíz R, García-Ruíz GM, Palomino C, Gutiérrez N, Vitale S, Ocaña-Moral S, Gutiérrez MV, Cubero JI, Torres AM (2013) A reference consensus genetic map for molecular markers and economically important traits in faba bean (Vicia faba L.). BMC Genom 14:932
Saxena RK, Varma Penmetsa RV, Upadhyaya HD, Kumar A, Carrasquilla-Garcia N, Schlueter JA, Farmer A, Whaley AM, Sarma BK, May GD, Cook DR, Varshney RK (2012) Large-scale development of cost-effective single-nucleotide polymorphism marker assays for genetic mapping in pigeon pea and comparative mapping in legumes. DNA Res 19:449–461
Semagn K, Babu R, Hearne S, Olsen M (2014) Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Mol Breed 33:1–14
Sharpe AG, Ramsay L, Sanderson L-A, Fedoruk MJ, Clarke WE, Li R, Kagale S, Vijayan P, Vandenberg A, Bett KE (2013) Ancient orphan crop joins modern era: gene-based SNP discovery and mapping in lentil. BMC Genom 14:192
Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293
Sjödin J (1971) Induced morphological variation in Vicia faba L. Hereditas 67:155–180
Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I (2010) Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–244
Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K, Kusakabe K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) Abiotic stress-inducible receptor-like kinases negatively control ABA signal in Arabidopsis. Plant J 70:599–613
Tayeh N, Bahrman N, Devaux R, Bluteau A, Prosperi JM, Delbreil B, Lejeune-Hénaut I (2013) A high-density genetic map of the Medicago truncatula major freezing tolerance QTL on chromosome 6 reveals colinearity with a QTL related to freezing damage on Pisum sativum linkage group VI. Mol Breed 32:279–289
Torres AM, Avila CM, Gutierrez N, Palomino C, Moreno MT, Cubero JI (2010) Marker-assisted selection in faba bean (Vicia faba L.). Field Crops Res 115:243–252
Torres AM, Avila CM, Stoddard FL, Cubero JI (2012) Faba bean. In: Torres AM, Cubero JI, Kole C, Pérez de la Vega M (eds) Genetics, genomics and breeding in crop plants: cool season food legumes. Science Pubs Inc, New Hampshire, pp 50–97
van Ooijen JW (1992) Accuracy of mapping quantitative trait loci in autogamous species. Theor Appl Genet 84:803–811
Varshney RK, Song C, Saxena RK, Azam S, Yu S et al (2013) Draft genome sequence of kabuli chickpea (Cicer arietinum): genetic structure and breeding constraints for crop improvement. Nat Biotech 31:240–246
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang S, Basten CJ, Zeng Z-B (2012) Windows QTL Cartographer 2.5. In: Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
Yan J, Yang X, Shah T, Sanchez-Villeda H, Li J, Warburton ML, Zhou Y, Crouch JH, Xu Y (2010) High-throughput SNP genotyping with the GoldenGate assay in maize. Mol Breed 25:441–451
Young ND, Debellé F, Oldroyd GED, Geurts R, Cannon SB et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524
Yu L, Chen X, Wang Z, Wang S, Wang Y, Zhu Q, Li S, Xiang C (2013) Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol 162:1378–1391
Zhao J, Gao Y, Zhang Z, Chen T, Guo W, Zhang T (2013) A receptor-like kinase gene (GbRLK) from Gossypium barbadense enhances salinity and drought-stress tolerance in Arabidopsis. BMC Plant Biol 13:110
Zhu H, Choi H-K, Cook DR, Shoemaker RC (2005) Bridging model and crop legumes through genomics. Plant Physiol 137:1189–1196
Acknowledgments
H. Khazaei expresses his gratitude to the Emil Aaltonen Foundation (Emil Aaltosen Säätiö) and Niemi-säätiö for their financial support. The project was further supported by the University of Helsinki, Niemi-Säätiö and by “Legume Futures (Legume-supported cropping systems for Europe)”, a collaborative research project funding from the European Union’s Seventh Programme for research, technological development and demonstration under Grant Agreement No. 245216. In addition, we thank Markku Tykkyläinen, Sanna Peltola, Sini Lindström and Stefano Zanotto for their assistance in the glasshouse work. We thank Prof. Wolfgang Link (Georg-August-University, Göttingen, Germany) for providing the seeds of the parental lines.
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Communicated by Glenn James Bryan.
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Khazaei, H., O’Sullivan, D.M., Sillanpää, M.J. et al. Use of synteny to identify candidate genes underlying QTL controlling stomatal traits in faba bean (Vicia faba L.). Theor Appl Genet 127, 2371–2385 (2014). https://doi.org/10.1007/s00122-014-2383-y
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DOI: https://doi.org/10.1007/s00122-014-2383-y