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, 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 non-grasses 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 non-autonomous signaling center that promotes inflorescence branching, an important component of yield in cereal grasses.

Genetic control of branching patterns in grass inflorescences

“…The proteins TASSELSHEATH1 (TSH1) and TSH4 repress inflorescence bracts; when both are mutated, bracts expand and axillary meristems are reduced or entirely absent ( Whipple et al, 2010 ; Xiao et al, 2021) . TSH1 is a GATA-domain zinc finger transcription factor orthologous to NECKLEAF1 (NL1) in rice and THIRD OUTER GLUME (TRD) of barley ( Houston et al, 2012 ), which have similar mutant phenotypes and together are the founding members of the NL1/TSH1/TRD (NTT) family of proteins.…”

“…Both TSH4 and TSH1 are expressed in the cryptic bract of inflorescence branches and act synergistically, with TSH4 upstream of TSH1 ( Xiao et al, 2021 ; Figure 4 ). Together they regulate the expression of LIGULELESS2 ( LG2 ), encoding a basic leucine zipper protein that regulates outgrowth of long branches among many other phenotypes ( Walsh and Freeling, 2002 ).…”

“…TSH1 is co-expressed with ZmYABBY15 , a gene expected to be expressed in all leaf-like organs, confirming that the minute structure is indeed a bract. Based on gene expression and mutant phenotypes, Xiao et al (2021) suggest that the maize SPL proteins UNBRANCHED2 (UB2) and UB3 may also help regulate TSH1 expression. UB2 and UB3 are co-orthologous to OsSPL14 ( Chuck et al, 2014 ) and may control allocation of cells to lateral organs in general.…”

“…Thus, bract suppression in the grasses must proceed by a mechanism quite different from that of Arabidopsis ( Whipple et al, 2010 ). NTT-like genes are expressed in boundary regions in outgroups of the grasses, but early in grass evolution TSH1 acquired SBP binding sites in its promoter, bringing it under the control of TSH4 and causing bract expression ( Xiao et al, 2021) . In this position, TSH1 retains its presumed ancestral developmental role of suppressing cell division and growth, as well as a possible role in signaling.…”

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

“…The full set of GA-regulated transcripts in tassels identified here (Figure 2) should provide a clearer picture of any changes in GA levels affected by these mutants. 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.…”