Abstract
Floret fertility is a key determinant of the number of grains per inflorescence in cereals. During the evolution of wheat (Triticum sp.), floret fertility has increased, such that current bread wheat (Triticum aestivum) cultivars set three to five grains per spikelet. However, little is known regarding the genetic basis of floret fertility. The locus Grain Number Increase 1 (GNI1) is shown here to be an important contributor to floret fertility. GNI1 evolved in the Triticeae through gene duplication. The gene, which encodes a homeodomain leucine zipper class I (HD-Zip I) transcription factor, was expressed most abundantly in the most apical floret primordia and in parts of the rachilla, suggesting that it acts to inhibit rachilla growth and development. The level of GNI1 expression has decreased over the course of wheat evolution under domestication, leading to the production of spikes bearing more fertile florets and setting more grains per spikelet. Genetic analysis has revealed that the reduced-function allele GNI-A1 contributes to the increased number of fertile florets per spikelet. The RNAi-based knockdown of GNI1 led to an increase in the number of both fertile florets and grains in hexaploid wheat. Mutants carrying an impaired GNI-A1 allele out-yielded WT allele carriers under field conditions. The data show that gene duplication generated evolutionary novelty affecting floret fertility while mutations favoring increased grain production have been under selection during wheat evolution under domestication.
| Original language | American English |
|---|---|
| Pages (from-to) | 5182-5187 |
| Number of pages | 6 |
| Journal | Proceedings of the National Academy of Sciences of the United States of America |
| Volume | 116 |
| Issue number | 11 |
| DOIs | |
| State | Published - 2019 |
Bibliographical note
Funding Information:15. Sukumaran S, Lopes M, Dreisigacker S, Reynolds M (2018) Genetic analysis of multi-environmental spring wheat trials identifies genomic regions for locus-specific trade- Materials and Methods Details about plant materials, QTL mapping, fine mapping, transformation, TILLING, yield trials, quantitative RT-PCR, in situ hybridization, RNA-seq, haplotype analysis, and phylogenetic analysis are in SI Appendix and Materials and Methods. Gene sequences generated in this study are available from the DNA Data Bank of Japan (DDBJ) under accession numbers AB711370–AB711394 (http://getentry.ddbj.nig.ac.jp/getentry/na/AB711370 and http://getentry.ddbj.nig.ac.jp/getentry/na/AB711394) and AB711888– AB711913 (http://getentry.ddbj.nig.ac.jp/getentry/na/AB711888 and http:// getentry.ddbj.nig.ac.jp/getentry/na/AB711913) and from the NCBI GenBank under accession numbers MH134165–MH134483. The RNA-seq data have been submitted to the European Nucleotide Archive under accession number PRJEB25119. ACKNOWLEDGMENTS. Grains of the RISL population were kindly provided by S. Xu and J. Faris [US Department of Agriculture (USDA) Agricultural Research Service (ARS)]. Y. Ono, F. Kobayashi, and H. Handa (National Agriculture and Food Research Organization) made available the DNA samples and grains of the cv. Kitahonami TILLING population. The winter bread wheat panel materials were a gift of M. Röder [Leibniz Institute of Plant Genetics and Crop Plant Research (IPK)]. We thank H. Tsuji (Yokohama City University) for providing the pANDA-b vector and the following institutions for providing germplasm: National BioResource Project-Wheat (Kyoto, Japan), the Nordic Genetic Resources Center (Alnarp, Sweden), IPK (Gatersleben, Germany), USDA (Aberdeen, ID), and the International Maize and Wheat Improvement Center (El Batán, Mexico). We acknowledge the excellent technical support given by S. Kikuchi (Chiba University), H. Koyama, M. Sakuma (National Institute of Agrobiological Sciences), and C. Trautewig and A. Fiebig (IPK). This research was financially supported by Genomics for Agricultural Innovation Program of the Ministry of Agriculture, Forestry, and Fisheries of Japan Grant TRS1002 (to S.S. and T.K.); a grant-in-aid from the Japan Society for the Promotion of Science (JSPS) Postdoctoral Fellow for Research Abroad (to S.S.); Grant-in-Aid for Young Scientists (B) 16K18635 (to S.S.); Chief Scientist of the Israel Ministry of Agriculture and Rural Development Grant 20-10-0066 (to Z.P.); US Agency for International Development Middle East Research and Cooperation Grant M34-037 (to Z.P.); and German Research Foundation Grant BL462/10. 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Funding Information:
ACKNOWLEDGMENTS. Grains of the RISL population were kindly provided by S. Xu and J. Faris [US Department of Agriculture (USDA) Agricultural Research Service (ARS)]. Y. Ono, F. Kobayashi, and H. Handa (National Agriculture and Food Research Organization) made available the DNA samples and grains of the cv. Kitahonami TILLING population. The winter bread wheat panel materials were a gift of M. Röder [Leibniz Institute of Plant Genetics and Crop Plant Research (IPK)]. We thank H. Tsuji (Yokohama City University) for providing the pANDA-b vector and the following institutions for providing germplasm: National BioResource Project-Wheat (Kyoto, Japan), the Nordic Genetic Resources Center (Alnarp, Sweden), IPK (Gatersleben, Germany), USDA (Aberdeen, ID), and the International Maize and Wheat Improvement Center (El Batán, Mexico). We acknowledge the excellent technical support given by S. Kikuchi (Chiba University), H. Koyama, M. Sakuma (National Institute of Agrobiological Sciences), and C. Trautewig and A. Fiebig (IPK). This research was financially supported by Genomics for Agricultural Innovation Program of the Ministry of Agriculture, Forestry, and Fisheries of Japan Grant TRS1002 (to S.S. and T.K.); a grant-in-aid from the Japan Society for the Promotion of Science (JSPS) Postdoctoral Fellow for Research Abroad (to S.S.); Grant-in-Aid for Young Scientists (B) 16K18635 (to S.S.); Chief Scientist of the Israel Ministry of Agriculture and Rural Development Grant 20-10-0066 (to Z.P.); US Agency for International Development Middle East Research and Cooperation Grant M34-037 (to Z.P.); and German Research Foundation Grant BL462/10. During parts of this study, T.S. received financial support from HEISENBERG Program of the German Research Foundation (DFG) Grant SCHN 768/8-1 and the IPK core budget.
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Keywords
- Duplication
- Floret fertility
- Grain number
- HD-Zip I transcription factor
- Wheat