Barley HISTIDINE KINASE 1 (HvHK1) coordinates transfer cell specification in the young endosperm

Abstract

SUMMARY Cereal endosperm represents the most important source of the world’s food; nevertheless, the molecular mechanisms underlying cell and tissue differentiation in cereal grains remain poorly understood. Endosperm cellularization commences at the maternal–filial intersection of grains and generates endosperm transfer cells (ETCs), a cell type with a prominent anatomy optimized for efficient nutrient transport. Barley HISTIDINE KINASE1 (HvHK1) was identified as a receptor component with spatially restricted expression in the syncytial endosperm where ETCs emerge. Here, we demonstrate its function in ETC fate acquisition using RNA interference‐mediated downregulation of HvHK1. Repression of HvHK1 impairs cell specification in the central ETC region and the development of transfer cell morphology, and consecutively defects differentiation of adjacent endosperm tissues. Coinciding with reduced expression of HvHK1, disturbed cell plate formation and fusion were observed at the initiation of endosperm cellularization, revealing that HvHK1 triggers initial cytokinesis of ETCs. Cell‐type‐specific RNA sequencing confirmed loss of transfer cell identity, compromised cell wall biogenesis and reduced transport capacities in aberrant cells and elucidated two‐component signaling and hormone pathways that are mediated by HvHK1. Gene regulatory network modeling was used to specify the direct targets of HvHK1; this predicted non‐canonical auxin signaling elements as the main regulatory links governing cellularization of ETCs, potentially through interaction with type‐B response regulators. This work provides clues to previously unknown molecular mechanisms directing ETC specification, a process with fundamental impact on grain yield in cereals.

Distinct Hormone Signalling-Modulation Activities Characterize Two Maize Endosperm-Specific Type-A Response Regulators

“…Interestingly, in a recent study in barley [ 40 ], an endosperm-specific histidine kinase was found to be essential for transfer cell differentiation. The gene does not cluster with ethylene or cytokinin receptors, but the analysis of RNAi kernels revealed regulatory links with atypical auxin signalling elements and canonical type-B response regulators.…”

Coordinated Transcriptome and Metabolome Analyses of a Barley hvhggt Mutant Reveal a Critical Role of Tocotrienols in Endosperm Starch Accumulation

“…During barley grain development, ETCs play crucial roles in assimilate transport and proper endosperm differentiation. 14,33 RNA interferencemediated downregulation of HvHK1 in barley impairs differentiation of ETC and consecutively causes defects in adjacent endosperm cellularization, resulting in low grain weight and starch content. 14 ZmMEG1 has been shown to be both necessary and sufficient for the establishment and differentiation of ETCs, promoting the nutrient uptake capacity of the seed and ultimately increasing biomass.…”

“…14,33 RNA interferencemediated downregulation of HvHK1 in barley impairs differentiation of ETC and consecutively causes defects in adjacent endosperm cellularization, resulting in low grain weight and starch content. 14 ZmMEG1 has been shown to be both necessary and sufficient for the establishment and differentiation of ETCs, promoting the nutrient uptake capacity of the seed and ultimately increasing biomass. 34 These findings support the essential role of ETCs in maternal and filial tissues.…”

“…Previous studies have identified a few genes with potential roles in triggering ETC differentiation in cereal grain development, such as END1, 12 ZmBETL1-4, 13 and HISTIDINE KINASE 1 (HvHK1). 14 ETCs, along with nucellar projection, mediate assimilate and nutrient transfer from maternal to filial tissues, including sugars, amino acids, hormones, micronutrients, and other solutes, which are crucial for endosperm growth and grain filling. 10 Despite the importance of the ETCs and aleurone cells, the starchy endosperm occupies most of the space in mature grains.…”

“…This suggests that the full functionality of ETCs is a prerequisite for proper endosperm differentiation. Previous studies have identified a few genes with potential roles in triggering ETC differentiation in cereal grain development, such as END1 , ZmBETL1-4 , and HISTIDINE KINASE 1 ( HvHK1 ) . ETCs, along with nucellar projection, mediate assimilate and nutrient transfer from maternal to filial tissues, including sugars, amino acids, hormones, micronutrients, and other solutes, which are crucial for endosperm growth and grain filling …”