Comprehensive analysis of Q gene near‐isogenic lines reveals key molecular pathways for wheat domestication and improvement

Abstract

† These authors contributed equally to this work. SUMMARYThe wheat AP2-like transcription factor gene Q has played a major role in domestication by conferring the free-threshing character and pleiotropically affecting numerous other traits. However, little information is known regarding the molecular mechanisms associated with the regulation of these traits by Q, especially for the structural determination of threshability. Here, transcriptome analysis of immature spike tissues in three lines nearly isogenic for Q revealed over 3000 differentially expressed genes (DEGs) involved in a number of pathways. Using phenotypic, microscopic, transcriptomic, and tissue-specific gene expression analyses, we demonstrated that Q governs threshability through extensive modification of wheat glumes including their structure, cell wall thickness, and chemical composition. Critical DEGs and pathways involved in secondary cell wall synthesis and regulation of the chemical composition of glumes were identified. We also showed that the mutation giving rise to the Q allele synchronized the expression of genes for micro-sporogenesis that affected pollen fertility, and may determine the final grain number for wheat spikes. Transcriptome dissection of genes and genetic pathways regulated by Q should further our understanding of wheat domestication and improvement.

The transcription factor TaLAX1 interacts with Q to antagonistically regulate grain threshability and spike morphogenesis in bread wheat

“…The previous section’s findings that Q and TaLAX1 physically interact to oppositely regulate domestication traits indicates that they might share some common target genes. Coincidentally, reported transcriptome data showed that some lignin biosynthesis‐related genes, including genes related to KNOTTED ARABIDOPSIS THALIANA7 ( KNAT7 ) and PHENYLALANIEN AMMONIA‐LYASA ( PAL1 ), were differentially expressed between the Q and q alleles (Zhang et al ., 2020). In this context, we speculated that TaLAX1 might also regulate the transcription of these lignin biosynthesis‐related genes.…”

“…Based on the findings that Q has transcriptional repression activity (Liu et al ., 2017b) and that the transcriptional expression of TaPAL1‐6B decreases in the Q allele (Zhang et al ., 2020), we further investigated the regulatory effect of Q on TaPAL1‐6B transcription. To this end, transient expression assays were performed in N .…”

“…KNAT7 , a lignin biosynthesis‐related gene, functions as a repressor of secondary cell wall formation, and loss function of KNAT7 results in thicker interfascicular fiber walls in Arabidopsis (Li et al ., 2012, 2014). Consistently, a recent study in wheat showed that the glume bases of the q allele were much thicker than those in the Q allele and the expression levels of TaKNAT7‐4D were lower in the q allele (Zhang et al ., 2020). In this study, we found that the glume bases of TaLAX1‐OE transgenic lines were much thicker than those in the control plants (Fig.…”

“…Several studies have shown that miR172 regulates the post‐transcriptional expression of Q in both tetraploid and hexaploid wheat (Debernardi et al ., 2017; Greenwood et al ., 2017; Liu et al ., 2017b). Recent transcriptome analyses showed that Q regulates the expression of lignin biosynthesis‐related genes (Zhang et al ., 2020). However, the molecular mechanisms of how Q regulates the wheat domestication traits remain elusive.…”

Molecular Cytogenetic Identification of Wheat-Aegilops Biuncialis 5Mb Disomic Addition Line with Tenacious and Black Glumes

“…tauschii [30][31][32] and 2E in Lophopyrum elongatum [33]. Zhang et al [34] demonstrated that Q governs threshability through extensive modification of wheat glumes including their structure, cell wall thickness and chemical composition. The glume color is an important taxonomic discriminator in wheat [35,36] and is associated with the crop's adaptability [37,38].…”