Barley HISTIDINE KINASE 1 (HvHK1) coordinates transfer cell specification in the young endosperm. (3rd July 2020)

• Record Type: Journal Article
• Authors: Hertig, Christian; Melzer, Michael; Rutten, Twan; Erbe, Stephan; Hensel, Götz; Kumlehn, Jochen; Weschke, Winfriede; Weber, Hans; Thiel, Johannes
• Is Part Of: Plant journal. Volume 103:Number 5(2020)
• Page Start: 1869
• Page End: 1884
• Publication Date: 2020-07-03
• Subjects: barley endosperm -- endosperm transfer cells/ETCs -- histidine kinase1/HvHK1 -- two‐component signaling/TCS -- cell specification -- regulatory networks -- auxin signaling; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.14875
• Languages: English
• ISSNs: 0960-7412

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. Significance Statement: Although endosperm transfer cells (ETCs) have a substantial impact on grain yield in cereals, the molecular basis and regulatory networks triggering differentiation of ETCs remain poorly understood. This work demonstrates that barley HISTIDINE KINASE1 directs ETC specification in the young endosperm by orchestrating distinct phosphorelay and hormone signaling modules.