Genomic Regions Associated with the Control of Flowering Time in Durum Wheat
Abstract
:1. Introduction
2. Results
2.1. Determination of Phenological Environments (PhEnv)
2.2. Analysis of Variance for G, G x E, and G x PhEnv
2.3. Marker-Trait Associations
2.4. Flowering Loci Identified among Landraces
2.5. Flowering Loci Identified among Modern Lines
2.6. Common Loci between Landraces and Modern Lines
2.7. Effect of Allelic Combinations
3. Discussion
3.1. Climatic Effect on the Control of Flowering Time
3.2. Known Loci Involved in the Control of Flowering Time in Durum Wheat
3.3. Identification of Novel Loci Involved in the Control of Flowering Time in Durum Wheat
3.4. Define Usable Alleles for Earliness via Haplotype Analysis of Multiple QTLs
4. Conclusions
5. Materials and Methods
5.1. Plant Material
5.2. Phenotyping
5.3. Genotyping
5.4. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Xynias, I.N.; Mylonas, I.; Korpetis, E.G.; Ninou, E.; Tsaballa, A.; Avdikos, I.D.; Mavromatis, A.G. Durum Wheat Breeding in the Mediterranean Region: Current Status and Future Prospects. Agronomy 2020, 10, 432. [Google Scholar] [CrossRef] [Green Version]
- Maccaferri, M.; Sanguineti, M.C.; Corneti, S.; Ortega, J.L.A.; Salem, M.B.; Bort, J.; DeAmbrogio, E.; del Moral, L.F.G.; Demontis, A.; El-Ahmed, A.; et al. Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum durum Desf.) across a wide range of water availability. Genetics 2008, 178, 489–511. [Google Scholar] [CrossRef] [Green Version]
- Pickett, A.A. Hybrid wheat-results and problems. Fortschr. Pflanz. AGRIS 1993, 15, 259. [Google Scholar]
- El Hassouni, K.; Belkadi, B.; Filali-Maltouf, A.; Tidiane-Sall, A.; Al-Abdallat, A.; Nachit, M.; Bassi, F.M. Loci controlling adaptation to heat stress occurring at the reproductive stage in durum wheat. Agronomy 2019, 9, 414. [Google Scholar] [CrossRef] [Green Version]
- Distelfeld, A.; Li, C.; Dubcovsky, J. Regulation of flowering in temperate cereals. Curr. Opin. Plant Biol. 2009, 12, 178–184. [Google Scholar] [CrossRef] [Green Version]
- Scarth, R.; Law, C.N. The control of the day-length response in wheat by the group 2 chromosomes. Z. Pflanz. 1984, 92, 140–150. [Google Scholar]
- Bullrich, L.; Appendino, M.; Tranquilli, G.; Lewis, S.; Dubcovsky, J. Mapping of a thermo-sensitive earliness per se gene on Triticum monococcum chromosome 1A m. TAG Theor. Appl. Genet. 2002, 105, 585–593. [Google Scholar] [CrossRef]
- Zikhali, M.; Griffiths, S. The Effect of Earliness per se (Eps) genes on Flowering Time in Bread Wheat. Advances in Wheat Genetics: From Genome to Field; Springer Japan: Tokyo, Japan, 2015; pp. 339–345. [Google Scholar]
- Appendino, M.L.; Slafer, G.A. Earliness per se and its dependence upon temperature in diploid wheat lines differing in the major gene Eps-Am1 alleles. J. Agric. Sci. 2003, 141, 149–154. [Google Scholar] [CrossRef] [Green Version]
- Chouard, P. Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. 1960, 11, 191–238. [Google Scholar] [CrossRef]
- Rawson, H.M.; Zajac, M.; Penrose, L.D.J. Effect of seedling temperature and its duration on development of wheat cultivars differing in vernalization response. F. Crop. Res. 1998, 57, 289–300. [Google Scholar] [CrossRef]
- Pugsley, A.T. Additional genes inhibiting winter habit in wheat. Euphytica 1972, 21, 547–552. [Google Scholar] [CrossRef]
- Kiss, T.; Balla, K.; Veisz, O.; Láng, L.; Bedő, Z.; Griffiths, S.; Isaac, P.; Karsai, I. Allele frequencies in the VRN-A1, VRN-B1 and VRN-D1 vernalization response and PPD-B1 and PPD-D1 photoperiod sensitivity genes, and their effects on heading in a diverse set of wheat cultivars (Triticum aestivum L.). Mol. Breed. 2014, 34, 297–310. [Google Scholar] [CrossRef] [Green Version]
- Iqbal, M.; Shahzad, A.; Ahmed, I. Allelic variation at the Vrn-A1, Vrn-B1, Vrn-D1, Vrn-B3 and Ppd-D1a loci of Pakistani spring wheat cultivars. Electron. J. Biotechnol. 2011, 14, 1–2. [Google Scholar] [CrossRef] [Green Version]
- Pugsley, A.T. A genetic analysis of the spring-winter habit of growth in wheat. Aust. J. Agric. Res. 1971, 22, 21–31. [Google Scholar] [CrossRef]
- Iqbal, M.; Navabi, A.; Yang, R.-C.; Salmon, D.F.; Spaner, D. Molecular characterization of vernalization response genes in Canadian spring wheat. Genome 2007, 50, 511–516. [Google Scholar] [CrossRef]
- Turner, A.S.; Faure, S.; Zhang, Y.; Laurie, D.A. The effect of day-neutral mutations in barley and wheat on the interaction between photoperiod and vernalization. Theor. Appl. Genet. 2013, 126, 2267–2277. [Google Scholar] [CrossRef] [Green Version]
- Yan, L.; Helguera, M.; Kato, K.; Fukuyama, S.; Sherman, J.; Dubcovsky, J. Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor. Appl. Genet. 2004, 109, 1677–1686. [Google Scholar] [CrossRef] [Green Version]
- Fu, D.; Szucs, P.; Yan, L.; Helguera, M.; Skinner, J.S.; Von Zitzewitz, J.; Hayes, P.M.; Dubcovsky, J.; Szűcs, P.; Yan, L.; et al. Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol. Genet. Genom. 2005, 273, 54–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yan, L.; Loukoianov, A.; Tranquilli, G.; Helguera, M.; Fahima, T.; Dubcovsky, J. Positional cloning of the wheat vernalization gene VRN1. Proc. Natl. Acad. Sci. USA 2003, 100, 6263–6268. [Google Scholar] [CrossRef] [Green Version]
- Turner, A.; Beales, J.; Faure, S.; Dunford, R.P.; Laurie, D.A. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 2005, 310, 1031–1034. [Google Scholar] [CrossRef]
- Ortiz, R.; Trethowan, R.; Ferrara, G.O.; Iwanaga, M.; Dodds, J.H.; Crouch, J.H.; Crossa, J.; Braun, H.-J. High yield potential, shuttle breeding, genetic diversity, and a new international wheat improvement strategy. Euphytica 2007, 157, 365–384. [Google Scholar] [CrossRef]
- Royo, C.; Dreisigacker, S.; Alfaro, C.; Ammar, K.; Villegas, D. Effect of Ppd-1 genes on durum wheat flowering time and grain filling duration in a wide range of latitudes. J. Agric. Sci. 2016, 154, 612–631. [Google Scholar] [CrossRef] [Green Version]
- Laurie, D.A. Comparative genetics of flowering time. Plant Mol. Biol. 1997, 35, 167–177. [Google Scholar] [CrossRef]
- McIntosh, R.A.; Yamazaki, Y.; Devos, K.M.; Dubcovsky, J.; Rogers, W.J.; Appels, R. Catalogue of gene symbols for wheat. Wheat Inf. Serv. 2003, 97, 27–37. [Google Scholar]
- Wilhelm, E.P.; Turner, A.S.; Laurie, D.A. Photoperiod insensitive Ppd-A1a mutations in tetraploid wheat (Triticum durum Desf.). Theor. Appl. Genet. 2009, 118, 285–294. [Google Scholar] [CrossRef]
- Kamran, A.; Iqbal, M.; Spaner, D. Flowering time in wheat (Triticum aestivum L.): A key factor for global adaptability. Euphytica 2014, 197, 1–26. [Google Scholar] [CrossRef]
- Royo, C.; Dreisigacker, S.; Soriano, J.M.; Lopes, M.S.; Ammar, K.; Villegas, D. Allelic Variation at the Vernalization Response (Vrn-1) and Photoperiod Sensitivity (Ppd-1) Genes and Their Association With the Development of Durum Wheat Landraces and Modern Cultivars. Front. Plant Sci. 2020, 11, 838. [Google Scholar] [CrossRef]
- Maccaferri, M.; Cane, M.A.; Sanguineti, M.C.; Salvi, S.; Colalongo, M.C.; Massi, A.; Clarke, F.; Knox, R.; Pozniak, C.J.; Clarke, J.M. A consensus framework map of durum wheat (Triticum durum Desf.) suitable for linkage disequilibrium analysis and genome-wide association mapping. BMC Genom. 2014, 15, 873. [Google Scholar] [CrossRef] [Green Version]
- Wilczek, A.M.; Burghardt, L.T.; Cobb, A.R.; Cooper, M.D.; Welch, S.M.; Schmitt, J. Genetic and physiological bases for phenological responses to current and predicted climates. Philos. Trans. R. Soc. London B Biol. Sci. 2010, 365, 3129–3147. [Google Scholar] [CrossRef] [Green Version]
- Würschum, T.; Rapp, M.; Miedaner, T.; Longin, C.F.H.; Leiser, W.L. Copy number variation of Ppd-B1 is the major determinant of heading time in durum wheat. BMC Genet. 2019, 20, 1–8. [Google Scholar] [CrossRef]
- Laurie, D.A.; Pratchett, N.; Snape, J.W.; Bezant, J.H. RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter× spring barley (Hordeum vulgare L.) cross. Genome 1995, 38, 575–585. [Google Scholar] [CrossRef]
- Craufurd, P.Q.; Wheeler, T.R. Climate change and the flowering time of annual crops. J. Exp. Bot. 2009, 60, 2529–2539. [Google Scholar] [CrossRef] [Green Version]
- Hemming, M.N.; Walford, S.A.; Fieg, S.; Dennis, E.S.; Trevaskis, B. Identification of high-temperature-responsive genes in cereals. Plant Physiol. 2012, 158, 1439–1450. [Google Scholar] [CrossRef] [Green Version]
- Villegas, D.; Alfaro, C.; Ammar, K.; Cátedra, M.; Crossa, J.; Moral, L.; Royo, C. Daylength, Temperature and Solar Radiation Effects on the Phenology and Yield Formation of Spring Durum Wheat. J. Agron. Crop Sci. 2015, 202. [Google Scholar] [CrossRef]
- Trevaskis, B.; Bagnall, D.J.; Ellis, M.H.; Peacock, W.J.; Dennis, E.S. MADS box genes control vernalization-induced flowering in cereals. Proc. Natl. Acad. Sci. USA 2003, 100, 13099–13104. [Google Scholar] [CrossRef] [Green Version]
- Loukoianov, A.; Yan, L.; Blechl, A.; Sanchez, A.; Dubcovsky, J. Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol. 2005, 138, 2364–2373. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.K.; Xiao, Y.G.; Zhang, Y.; Xia, X.C.; Dubcovsky, J.; He, Z.H. Allelic variation at the vernalization genes Vrn-A1, Vrn-B1, Vrn-D1, and Vrn-B3 in Chinese wheat cultivars and their association with growth habit. Crop Sci. 2008, 48, 458–470. [Google Scholar] [CrossRef] [Green Version]
- Basualdo, J.; Díaz, M.L.; Cuppari, S.; Cardone, S.; Soresi, D.; Camargo, G.P.; Carrera, A. Allelic variation and differential expression of VRN-A1 in durum wheat genotypes varying in the vernalization response. Plant Breed. 2015, 134, 520–528. [Google Scholar] [CrossRef]
- Konopatskaia, I.; Vavilova, V.; Kondratenko, E.Y.; Blinov, A.; Goncharov, N.P. VRN1 genes variability in tetraploid wheat species with a spring growth habit. BMC Plant Biol. 2016, 16, 244. [Google Scholar] [CrossRef] [Green Version]
- Pascual, L.; Ruiz, M.; López-Fernández, M.; Pérez-Peña, H.; Benavente, E.; Vázquez, J.F.; Sansaloni, C.; Giraldo, P. Genomic analysis of Spanish wheat landraces reveals their variability and potential for breeding. BMC Genom. 2020, 21, 122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chu, C.-G.; Tan, C.T.; Yu, G.-T.; Zhong, S.; Xu, S.S.; Yan, L. A Novel Retrotransposon Inserted in the Dominant Vrn-B1 Allele Confers Spring Growth Habit in Tetraploid Wheat (Triticum turgidum L.). G3 Genes Genomes Genet. 2011, 1, 637–645. [Google Scholar] [CrossRef] [Green Version]
- Shcherban, A.; Emtseva, M.; Efremova, T. Molecular genetical characterization of vernalization genes Vrn-A1, Vrn-B1 and Vrn-D1 in spring wheat germplasm from Russia and adjacent regions. Cereal Res. Commun. 2012, 40, 351–361. [Google Scholar] [CrossRef] [Green Version]
- Trevaskis, B.; Hemming, M.N.; Dennis, E.S.; Peacock, W.J. The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci. 2007, 12, 352–357. [Google Scholar] [CrossRef]
- Roncallo, P.F.; Akkiraju, P.C.; Cervigni, G.L.; Echenique, V.C. QTL mapping and analysis of epistatic interactions for grain yield and yield-related traits in Triticum turgidum L. var. durum. Euphytica 2017, 213. [Google Scholar] [CrossRef]
- Tanio, M.; Kato, K. Development of near-isogenic lines for photoperiod-insensitive genes, Ppd-B1 and Ppd-D1, carried by the Japanese wheat cultivars and their effect on apical development. Breed. Sci. 2007, 57, 65–72. [Google Scholar] [CrossRef] [Green Version]
- Shaw, L.M.; Turner, A.S.; Laurie, D.A. The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). Plant J. 2012, 71, 71–84. [Google Scholar] [CrossRef] [PubMed]
- Würschum, T.; Boeven, P.H.G.; Langer, S.M.; Longin, C.F.H.; Leiser, W.L. Multiply to conquer: Copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat. BMC Genet. 2015, 16, 96. [Google Scholar] [CrossRef] [Green Version]
- Bentley, A.R.; Turner, A.S.; Gosman, N.; Leigh, F.J.; Maccaferri, M.; Dreisigacker, S.; Greenland, A.; Laurie, D.A. Frequency of photoperiod-insensitive Ppd-A1a alleles in tetraploid, hexaploid and synthetic hexaploid wheat germplasm. Plant Breed. 2011, 130, 10–15. [Google Scholar] [CrossRef]
- Wang, S.; Xu, S.; Chao, S.; Sun, Q.; Liu, S.; Xia, G. A genome-wide association study of highly heritable agronomic traits in durum wheat. Front. Plant Sci. 2019, 10, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Maccaferri, M.; Sanguineti, M.C.; Demontis, A.; El-Ahmed, A.; Garcia del Moral, L.; Maalouf, F.; Nachit, M.; Nserallah, N.; Ouabbou, H.; Rhouma, S. Association mapping in durum wheat grown across a broad range of water regimes. J. Exp. Bot. 2010, 62, 409–438. [Google Scholar] [CrossRef] [Green Version]
- Giunta, F.; De Vita, P.; Mastrangelo, A.M.; Sanna, G.; Motzo, R. Environmental and genetic variation for yield-related traits of durum wheat as affected by development. Front. Plant Sci. 2018, 9, 1–19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maccaferri, M.; Harris, N.S.; Twardziok, S.O.; Pasam, R.K.; Gundlach, H.; Spannagl, M.; Ormanbekova, D.; Lux, T.; Prade, V.M.; Milner, S.G. Durum wheat genome highlights past domestication signatures and future improvement targets. Nat. Genet. 2019, 51, 885–895. [Google Scholar] [CrossRef] [Green Version]
- Kamran, A.; Iqbal, M.; Navabi, A.; Randhawa, H.; Pozniak, C.; Spaner, D. Earliness per se QTLs and their interaction with the photoperiod insensitive allele Ppd-D1a in the Cutler × AC Barrie spring wheat population. Theor. Appl. Genet. 2013, 126, 1965–1976. [Google Scholar] [CrossRef]
- Sanna, G.; Giunta, F.; Motzo, R.; Mastrangelo, A.M.; De Vita, P. Genetic variation for the duration of pre-anthesis development in durum wheat and its interaction with vernalization treatment and photoperiod. J. Exp. Bot. 2014, 65, 3177–3188. [Google Scholar] [CrossRef] [Green Version]
- Milner, S.G.; Maccaferri, M.; Huang, B.E.; Mantovani, P.; Massi, A.; Frascaroli, E.; Tuberosa, R.; Salvi, S. A multiparental cross population for mapping QTL for agronomic traits in durum wheat (Triticum turgidum ssp. durum). Plant Biotechnol. J. 2016, 14, 735–748. [Google Scholar] [CrossRef] [Green Version]
- Kabbaj, H.; Sall, A.T.; Al-Abdallat, A.; Geleta, M.; Amri, A.; Filali-Maltouf, A.; Belkadi, B.; Ortiz, R.; Bassi, F.M. Genetic diversity within a global panel of durum wheat (Triticum durum) landraces and modern germplasm reveals the history of alleles exchange. Front. Plant Sci. 2017, 8, 1277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Klepper, B.; Rickman, R.W.; Zuzel, J.F.; Waldman, S.E. Use of growing degree days to project sample dates for cereal crops. Agron. J. 1988, 80, 850–852. [Google Scholar] [CrossRef]
- Sall, A.T.; Bassi, F.M.; Cisse, M.; Gueye, H.; Ndoye, I.; Filali-Maltouf, A.; Ortiz, R. Durum wheat breeding: In the heat of the Senegal river. Agriculture 2018, 8, 99. [Google Scholar] [CrossRef] [Green Version]
- Bassi, F.M.; Brahmi, H.; Sabraoui, A.; Amri, A.; Nsarellah, N.; Nachit, M.M.; Al-Abdallat, A.; Chen, M.S.; Lazraq, A.; El Bouhssini, M. Genetic identification of loci for Hessian fly resistance in durum wheat. Mol. Breed. 2019, 39. [Google Scholar] [CrossRef] [Green Version]
- Bradbury, P.J.; Zhang, Z.; Kroon, D.E.; Casstevens, T.M.; Ramdoss, Y.; Buckler, E.S. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 2007, 23, 2633–2635. [Google Scholar] [CrossRef]
- Murtagh, F.; Legendre, P. Ward’s hierarchical agglomerative clustering method: Which algorithms implement Ward’s criterion? J. Classif. 2014, 31, 274–295. [Google Scholar] [CrossRef] [Green Version]
- Falconer, D.S.; Mackay, T.F.C.; Frankham, R. Introduction to quantitative genetics (4th edn). TRENDS Genet. 1996, 12, 280. [Google Scholar]
- Burton, G.W.; de Devane, E.H. Estimating heritability in tall fescue (Festuca arundinacea) from replicated clonal material 1. Agron. J. 1953, 45, 478–481. [Google Scholar] [CrossRef]
- Duggal, P.; Gillanders, E.M.; Holmes, T.N.; Bailey-Wilson, J.E. Establishing an adjusted p-value threshold to control the family-wide type 1 error in genome wide association studies. BMC Genom. 2008, 9, 516. [Google Scholar] [CrossRef] [Green Version]
- Pearson, K.X. Contributions to the mathematical theory of evolution.—II. Skew variation in homogeneous material. Philos. Trans. R. Soc. 1895, 186, 343–414. [Google Scholar]
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis; Springer: Berlin/Heidelberg, Germany, 2016; ISBN 3319242776. [Google Scholar]
PhEnv. | Location | Loci | Expected Effect | Differential Effects at Main Flowering Loci between Phenv | ||
---|---|---|---|---|---|---|
1 | 2 | 3 | ||||
1 | Morocco | Ppd | Yes | |||
Vrn | Weak | |||||
2 | Lebanon | Ppd | Yes | Vrn: weak vs. strong | ||
Vrn | Yes | |||||
3 | Senegal and Mauritania | Ppd | 12h | Ppd: 12 h vs. normal Vrn: no vs. weak | Ppd: 12 h vs. normal Vrn: no vs. strong | |
Vrn | No | |||||
4 | Lebanon summer | Ppd | Shortening | Ppd: short vs. normal Vrn: no vs. weak | Ppd: short vs. normal Vrn: no vs. strong | Ppd: 12 h vs. shortening |
Vrn | No |
QTL | Marker | Chr. | Germplasm | PhEnv 1 | PhEnv 2 | PhEnv 3 | PhEnv 4 | Across PhEnv |
---|---|---|---|---|---|---|---|---|
Q.ICD.Ppd-05 | Ppd-B1 | 2B | Modern | ● | ● | |||
Landrace | ● | ● | ||||||
Q.ICD.Vrn-11 | Vrn-A1 | 5A | Modern | ●●● | ●● | ● | ||
Landrace | ●● | |||||||
Q.ICD.Vrn-16 | Vrn-A3 | 7A | Modern | ● | ||||
Landrace | ● | |||||||
Q.ICD.Eps-03 | AX-94460586 | 2A | Modern | ● | ● | |||
Landrace | ●● | ● | ||||||
Q.ICD.Eps-09 | AX-95630216 | 4A | Modern | ● | ||||
Landrace | ●● | |||||||
Q.ICD.Ppd-10 | AX-94554200 | 4B | Modern | ●● | ● | |||
Landrace | ●●●● | |||||||
Q.ICD.Vrn-15 | AX-94711490 | 6B | Modern | ● | ● | ● | ●● | |
Landrace | ● |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gupta, P.; Kabbaj, H.; El Hassouni, K.; Maccaferri, M.; Sanchez-Garcia, M.; Tuberosa, R.; Bassi, F.M. Genomic Regions Associated with the Control of Flowering Time in Durum Wheat. Plants 2020, 9, 1628. https://doi.org/10.3390/plants9121628
Gupta P, Kabbaj H, El Hassouni K, Maccaferri M, Sanchez-Garcia M, Tuberosa R, Bassi FM. Genomic Regions Associated with the Control of Flowering Time in Durum Wheat. Plants. 2020; 9(12):1628. https://doi.org/10.3390/plants9121628
Chicago/Turabian StyleGupta, Priyanka, Hafssa Kabbaj, Khaoula El Hassouni, Marco Maccaferri, Miguel Sanchez-Garcia, Roberto Tuberosa, and Filippo Maria Bassi. 2020. "Genomic Regions Associated with the Control of Flowering Time in Durum Wheat" Plants 9, no. 12: 1628. https://doi.org/10.3390/plants9121628