Boundary domain genes were recruited to suppress bract growth and promote branching in maize

Abstract

Grass inflorescence development is diverse and complex and involves sophisticated but poorly understood interactions of genes regulating branch determinacy and leaf growth. Here, we use a combination of transcript profiling and genetic and phylogenetic analyses to investigate tasselsheath1 ( tsh1 ) and tsh4 , two maize genes that simultaneously suppress inflorescence leaf growth and promote branching. We identify a regulatory network of inflorescence leaf suppression that involves the phase change gene tsh4 upstream of tsh1 and the ligule identity gene liguleless2 ( lg2 ). We also find that a series of duplications in the tsh1 gene lineage facilitated its shift from boundary domain in nongrasses to suppressed inflorescence leaves of grasses. Collectively, these results suggest that the boundary domain genes tsh1 and lg2 were recruited to inflorescence leaves where they suppress growth and regulate a nonautonomous signaling center that promotes inflorescence branching, an important component of yield in cereal grasses.

Dynamic transcriptome landscape of developing maize ear

“…The Liguleless2 ( LG2 , Zm00001eb147220 ) was a marker of non‐epidermis of determinate lateral organ expressed at IM and SB region and went down at SPM segments. LG2 was once reported as a sign of ligule and auricle formation (Walsh et al., 1998), and then was proved to regulate bract suppression and branch meristem determinacy downstream Tasselsheath1 ( TSH1 , Zm00001eb296770 ) and Tasselsheath4 ( TSH4 , Zm00001eb316740 ) (Xiao et al., 2022), which showed nearly the same expression pattern as LG2 in our work. The xylem markers BIF1 and PIN1a were synergistically involved in auxin transportation, which was both IM‐specific.…”

Transcriptional responses to gibberellin in the maize tassel and control by DELLA domain proteins

“…Of the 366 GA‐regulated genes (Table S3), 332 were reported by Xiao et al. ( 2022 ), and the gene expression directions of 218, 181, and 217 genes were consistent with low GA signaling in tsh1 , tsh4 , and their double mutant, respectively. Thus, the tsh mutants appear to have low GA signaling, resulting in decreased accumulation of GA catabolic enzyme transcripts as well as other GA‐induced genes.…”

“…A recent study identified downregulation of the GA‐inactivating GA2‐OXs in tasselsheath1 ( tsh1 ), tsh4 , and their double mutants (Xiao et al., 2022 ). The TSH1 and TSH4 genes encode transcription factors that control meristem determinacy, branching, and bract formation (Bommert & Whipple, 2018 ; Chuck et al., 2010 ; Whipple et al., 2010 ).…”

The maize preligule band is subdivided into distinct domains with contrasting cellular properties prior to ligule outgrowth

“…In situ hybridization showed CUC2-like transcripts were detected throughout the PLB early in development, but later became restricted to the distal zone of the PLB, where a cleft will form as the ligule grows out. Xiao et al (2022) further supported the link between liguleless2 and boundary-associated gene expression in the context of bract suppression in the inflorescence. These patterns of gene expression support the idea that the PLB functions as a boundary domain.…”

“…Cell fate, as well as differences in the rate and direction of cell division and expansion, are patterned along these axes. The boundary is maintained at the base of the organ throughout development and can be recapitulated at other locations on the developing organ (Bouré et al, 2022; Johnston et al, 2014; Nahar et al, 2012; Xiao et al, 2022).…”