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

Abstract

Significance Grain number is a key determinant of cereal grain yield, but its underlying genetic basis in wheat remains undefined. This study demonstrates a direct association between increased floret fertility, higher grain number per spike, and higher plot yields of field-grown wheat. The GNI1 gene, encoding an HD-Zip I transcription factor, was identified as responsible for increased floret fertility. The WT allele acts specifically during rachilla development, with its product serving to lower grain yield potential; in contrast, the reduced-function variant increased both floret and grain number. GNI1 evolved through gene duplication in the Triticeae, and its mutations have been under parallel selection in both wheat and barley over the course of domestication. 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.