Barley SIX-ROWED SPIKE3 encodes a putative Jumonji C-type H3K9me2/me3 demethylase that represses lateral spikelet fertility

Abstract

The barley inflorescence (spike) comprises a multi-noded central stalk (rachis) with tri-partite clusters of uni-floretted spikelets attached alternately along its length. Relative fertility of lateral spikelets within each cluster leads to spikes with two or six rows of grain, or an intermediate morphology. Understanding the mechanisms controlling this key developmental step could provide novel solutions to enhanced grain yield. Classical genetic studies identified five major SIX-ROWED SPIKE (VRS) genes, with four now known to encode transcription factors. Here we identify and characterise the remaining major VRS gene, VRS3, as encoding a putative Jumonji C-type H3K9me2/me3 demethylase, a regulator of chromatin state. Exploring the expression network modulated by VRS3 reveals specific interactions, both with other VRS genes and genes involved in stress, hormone and sugar metabolism. We show that combining a vrs3 mutant allele with natural six-rowed alleles of VRS1 and VRS5 leads to increased lateral grain size and greater grain uniformity.

Genetic pathways controlling inflorescence architecture and development in wheat and barley

“…This conclusion is supported by a previous study demonstrating that reduced levels of GA extend the duration of inflorescence development and delay flowering in barley (Boden et al ). These studies implicate hormones as important contributors to spikelet row‐type architecture and inflorescence development in barley, which is supported by genome‐wide expression analysis in vrs3 mutants that showed differential expression of genes involved in cytokinin and jasmonic acid metabolism, relative to wild‐type plants (Bull et al ; van Esse et al ; Youssef et al ). Taken together, these results suggest that adjustments to the levels and distribution of hormones, during inflorescence development, can be used to generate diverse inflorescence architectures in barley (Boden ).…”

“…Expression of Vrs4 is detected earlier than Vrs1 , and is localized predominantly within the lateral spikelet primordia during early developmental stages, suggesting that VRS4 protein regulates lateral spikelet fertility by acting upstream of Vrs1 (Koppolu et al ). Similarly, Vrs1 expression is reduced in vrs3 mutants that contain mutations within a gene that encodes a histone demethylase, which is predicted to facilitate activation of Vrs1 by removing repressive methyl marks and acting as a positive regulator of Vrs4 (van Esse et al ; Bull et al ). Taken together, these findings indicate that Vrs3 and Vrs4 regulate row‐type architecture of the barley inflorescence by converging to positively regulate transcription of Vrs1 .…”

“…However, recent evidence suggests that formation of the lateral spikelets may also influence pre‐harvest as well as grain dispersal and germination traits, such as grain development. For example, the extremely suppressed lateral spikelet development of the deficiens mutant facilitates enlarged grain size for the central spikelet, and introgression of mutant vrs3 alleles into six‐rowed backgrounds that contain loss‐of‐function vrs1 and vrs5 alleles improves uniformity of grain size produced by the lateral spikelets, relative to the central spikelet (Bull et al ; Sakuma et al ). It remains to be determined how these alleles of the row‐type architecture genes affect grain size; however, this effect may be associated with altered assimilate partitioning or reduced competition between the central and lateral spikelets (Sakuma et al ).…”

Developmental pathways for shaping spike inflorescence architecture in barley and wheat

“…Genetics and gene expression analyses suggest that HvRA2 regulates the barley row‐type pathway by promoting VRS1 transcription (Koppolu et al ). Unlike other row‐type genes, which encode transcription factors, VRS3 codes for an enzyme, a putative Jumonji C‐type (JMJC) H3K9me2/3 histone demethylase (HvJMJC) (Bull et al ; van Esse et al ). Interestingly, VRS3 appears to promote the transcription of all known row‐type genes supposedly by clearing repressive chromatin methylation marks (Bull et al ; van Esse et al ) (Figure G).…”

Interaction between row‐type genes in barley controls meristem determinacy and reveals novel routes to improved grain

“…Six‐rowed barley originated with multiple natural recessive vrs1 alleles (Tanno et al ., ), which are now accompanied by a natural allele of vrs5 ( Int‐c.a ) that confers improved lateral grain fill in six‐row cultivars (Harlan, ; Lundqvist et al ., ). The three other major recessive row‐type alleles are not prevalent in current six‐row cultivars (Koppolu et al ., ; Bull et al ., ; Youssef et al ., ).…”