GNI-A1 mediates trade-off between grain number and grain weight in tetraploid wheat
- 362 Downloads
Wild emmer allele of GNI-A1 ease competition among developing grains through the suppression of floret fertility and increase grain weight in tetraploid wheat.
Grain yield is a highly polygenic trait determined by the number of grains per unit area, as well as by grain weight. In wheat, grain number and grain weight are usually negatively correlated. Yet, the genetic basis underlying trade-off between the two is mostly unknown. Here, we fine-mapped a grain weight QTL using wild emmer introgressions in a durum wheat background and showed that grain weight is associated with the GNI-A1 gene, a regulator of floret fertility. In-depth characterization of grain number and grain weight indicated that suppression of distal florets by the wild emmer GNI-A1 allele increases weight of proximal grains in basal and central spikelets due to alteration in assimilate distribution. Re-sequencing of GNI-A1 in tetraploid wheat demonstrated the rich allelic repertoire of the wild emmer gene pool, including a rare allele which was present in two gene copies and contained a nonsynonymous mutation in the C-terminus of the protein. Using an F2 population generated from a cross between wild emmer accessions Zavitan, which carries the rare allele, and TTD140, we demonstrated that this unique polymorphism is associated with grain weight, independent of grain number. Moreover, we showed, for the first time, that GNI-A1 proteins are transcriptional activators and that selection targeted compromised activity of the protein. Our findings expand the knowledge of the genetic basis underlying trade-off between key yield components and may contribute to breeding efforts for enhanced grain yield.
We highly appreciate the excellent technical support of the Peleg laboratory members. Specially, we thank N. Teboul for drawing in Fig. 4. This research was supported by the Chief Scientist of the Israel Ministry of Agriculture and Rural Development (Grant #12-01-0005) and the US Agency for International Development Middle East Research and Cooperation (Grant # M34-037).
Author contribution statement
G.G., A.M., A.D. and Z.P. designed the research. G.G., I.A., A.P., G.Z. and T.A-A. performed experiments. G.G., G.Z. and Z.P. analyzed the data. G.G. and Z.P. wrote the manuscript with contributions from all coauthors.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW, Golan G, Deek J, Ben-Zvi B, Ben-Zvi G, Himmelbach A, MacLachlan RP, Sharpe AG, Fritz A, Ben-David R, Budak H, Fahima T, Korol A, Faris JD, Hernandez A, Mikel MA, Levy AA, Steffenson B, Maccaferri M, Tuberosa R, Cattivelli L, Faccioli P, Ceriotti A, Kashkush K, Pourkheirandish M, Komatsuda T, Eilam T, Sela H, Sharon A, Ohad N, Chamovitz DA, Mayer KFX, Stein N, Ronen G, Peleg Z, Pozniak CJ, Akhunov ED, Distelfeld A (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97CrossRefGoogle Scholar
- Fahy B, Siddiqui H, David LC, Powers SJ, Borrill P, Uauy C, Smith AM (2018) Final grain weight is not limited by the activity of key starch-synthesising enzymes during grain filling in wheat. J Exp Bot 69:5461–5475Google Scholar
- Harlan JR (1992) Crops and man, 2nd edn. American Society of Agronomy and Crop Science Society of America, MadisonGoogle Scholar
- Horovitz A (1998) The soil seed bank of wild emmer. In: Zeneirei N, Kaya Z, Anikster Y, Adams WT (eds) Proceedings of the international symposium on in‐situ conservation of plant genetic diversity. Central Research Institute of Field Crops, AnkaraGoogle Scholar
- Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, Lundqvist U, Fujimura T, Matsuoka M, Matsumoto T, Yano M (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci USA 104:1424–1429CrossRefGoogle Scholar
- Maccaferri M, Harris NS, Twardziok SO, Pasam RK, Gundlach H, Spannagl M, Ormanbekova D, Lux T, Prade VM, Milner SG, Himmelbach A, Mascher M, Bagnaresi P, Faccioli P, Cozzi P, Lauria M, Lazzari B, Stella A, Manconi A, Gnocchi M, Moscatelli M, Avni R, Deek J, Biyiklioglu S, Frascaroli E, Corneti S, Salvi S, Sonnante G, Desiderio F, Marè C, Crosatti C, Mica E, Özkan H, Kilian B, De Vita P, Marone D, Joukhadar R, Mazzucotelli E, Nigro D, Gadaleta A, Chao S, Faris JD, Melo ATO, Pumphrey M, Pecchioni N, Milanesi L, Wiebe K, Ens J, MacLachlan RP, Clarke JM, Sharpe AG, Koh CS, Liang KYH, Taylor GJ, Knox R, Budak H, Mastrangelo AM, Xu SS, Stein N, Hale I, Distelfeld A, Hayden MJ, Tuberosa R, Walkowiak S, Mayer KFX, Ceriotti A, Pozniak CJ, Cattivelli L (2019) Durum wheat genome highlights past domestication signatures and future improvement targets. Nat Genet 51:885–895CrossRefGoogle Scholar
- Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
- Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-FF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071Google Scholar
- Peleg Z, Saranga Y, Krugman T, Abbo S, Nevo E, Fahima T (2008) Allelic diversity associated with aridity gradient in wild emmer wheat populations. Plant Cell Environ 31:39–49Google Scholar
- Sakuma S, Lundqvist U, Kakei Y, Thirulogachandar V, Suzuki T, Hori K, Wu J, Tagiri A, Rutten T, Koppolu R, Shimada Y, Houston K, Thomas WTB, Waugh R, Schnurbusch T, Komatsuda T (2017) Extreme suppression of lateral floret development by a single amino acid change in the VRS1 transcription factor. Plant Physiol 175:1720–1731CrossRefGoogle Scholar
- Sakuma S, Golan G, Guo Z, Ogawa T, Tagiri A, Sugimoto K, Bernhardt N, Brassac J, Mascher M, Hensel G, Ohnishi S, Jinno H, Yamashita Y, Ayalon I, Peleg Z, Schnurbusch T, Komatsuda T (2019) Unleashing floret fertility in wheat through the mutation of a homeobox gene. Proc Natl Acad Sci USA 116:5182–5187CrossRefGoogle Scholar
- Stranger BE, Forrest MS, Dunning M, Ingle CE, Beazley C, Thorne N, Redon R, Bird CP, de Grassi A, Lee C, Tyler-Smith C, Carter N, Scherer SW, Tavaré S, Deloukas P, Hurles ME, Dermitzakis ET (2007) Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science 315:848–853CrossRefGoogle Scholar
- Xiao W (2006) Yeast protocols. Humana Press, TotowaGoogle Scholar