Unleashing floret fertility in wheat through the mutation of a homeobox gene.

Martin Mascher, Takao Komatsuda, Thorsten Schnurbusch, Zvi Peleg, Idan Ayalon, Yoko Yamashita, Hironobu Jinno, Shizen Ohnishi, Goetz Hensel, Shun Sakuma, Jonathan Brassac, Nadine Bernhardt, Kazuhiko Sugimoto, Akemi Tagiri, Taiichi Ogawa, Zifeng Guo, Guy Golan

Journal: Proceedings of the National Academy of Sciences of the United States of America 2019;116(11):5182-5187

PMID: 30792353

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Abstract

Floret fertility is a key determinant of the number of grains per inflorescence in cereals. During the evolution of wheat ( sp.), floret fertility has increased, such that current bread wheat () cultivars set three to five grains per spikelet. However, little is known regarding the genetic basis of floret fertility. The locus () is shown here to be an important contributor to floret fertility. 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 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 contributes to the increased number of fertile florets per spikelet. The RNAi-based knockdown of led to an increase in the number of both fertile florets and grains in hexaploid wheat. Mutants carrying an impaired 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.

Address: Agrogenomics Research Center, National Institute of Agrobiological Sciences, 305-8602 Tsukuba, Japan; [email protected] [email protected] [email protected].; Independent HEISENBERG Research Group Plant Architecture, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany.; Faculty of Agriculture, Tottori University, 680-8553 Tottori, Japan.; The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, 7610001 Rehovot, Israel.; Agrogenomics Research Center, National Institute of Agrobiological Sciences, 305-8602 Tsukuba, Japan.; Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 305-8518 Tsukuba, Japan.; Institute of Crop Science, National Agriculture and Food Research Organization, 305-8518 Tsukuba, Japan.; Research Group Experimental Taxonomy, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany.; Independent Research Group Domestication Genomics, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany.; German Centre for Integrative Biodiversity Research Halle-Jena-Leipzig, 04103 Leipzig, Germany.; Research Group Plant Reproductive Biology, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany.; Kitami Agricultural Experiment Station, Hokkaido Research Organization, 099-1496 Kunneppu, Japan.; Central Agricultural Experiment Station, Hokkaido Research Organization, 069-1395 Naganuma, Japan.; Independent HEISENBERG Research Group Plant Architecture, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany; [email protected] [email protected] [email protected].; Institute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, 06120 Halle, Germany.

DOI: 10.1073/pnas.1815465116

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MeSH Terms: Alleles, Cloning, Molecular, Evolution, Molecular, Fertility, Flowers, Gene Expression Regulation, Plant, Genes, Homeobox, Genes, Plant, Genetic Variation, Mutation, Plant Proteins, Ploidies, Quantitative Trait Loci, RNA, Messenger, Triticum