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

Authors: Zhang, Zengcui; LI, AILI - Chinese Academy Of Agricultural Sciences; SONG, GAOYUAN - Chinese Academy Of Agricultural Sciences; GENG, SHUAIFENG - Chinese Academy Of Agricultural Sciences; GILL, BIKRAM - Kansas State University; Faris, Justin; MAO, LONG - Chinese Academy Of Agricultural Sciences

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/12/2019
Publication Date: 11/28/2019
Citation: Zhang, Z., Li, A., Song, G., Geng, S., Gill, B.S., Faris, J.D., Mao, L. 2019. Comprehensive analysis of Q gene near isogenic lines reveals key molecular pathways for wheat domestication and improvement. Plant Journal. 102:299-310. https://doi.org/10.1111/tpj.14624.
DOI: https://doi.org/10.1111/tpj.14624

Interpretive Summary: A mutation occurred naturally about 10,000 years ago in a single wheat gene known as the q gene. The mutated gene, referred to as Q, influenced many developmental traits associated with domestication, one of the more important being the free-threshing, or naked seed, character. Knowing the molecular and physiological mechanisms regulated by the Q gene to govern plant development and grain threshability may lead to novel methods for wheat improvement. Using molecular, microscopic, and genetic studies, researchers found that the Q gene is responsible for regulating the activity of several thousand other wheat genes, many of which are involved in the development and chemical composition of plant structures known as glumes, which function to retain the grains on the wheat plant. The mutation that formed Q caused the glumes to be thin and fragile, and to hold the grains loosely allowing them to be easily liberated from the hulls. The researchers also found that the Q gene led to increased plant fertility, thereby increasing grain yields. This research sheds light on the domestication process, the role of the Q gene in governing plant development and domestication traits, and the genes and genetic networks under the influence of the master regulatory gene Q. This knowledge will allow researchers to develop novel strategies to improve wheat varieties more efficiently.

Technical Abstract: A single point mutation in the microRNA172 binding site of the wheat AP2-like transcription factor gene known as Q played a major role in domestication by conferring the free-threshing character and pleiotropically affecting numerous other traits. However, little is known regarding the molecular mechanisms associated with the regulation of these traits by Q or the structural determinants of threshability. Here, transcriptome analysis of immature spike tissues in three lines nearly isogenic for Q revealed over 3,000 differentially expressed genes (DEGs) involved in a number of pathways. Phenotypic, microscopic, transcriptomic, and tissue-specific gene expression analyses together demonstrated that Q governs threshability through extensive modification of wheat glumes including their structure, cell wall thickness and chemical composition. The critical DEGs involved in secondary cell wall synthesis and regulation of the chemical composition of glumes were identified. In addition to threshability, we found that the mutation that gave rise to the Q allele also led to the up-regulation of genes for improved anther and pollen development and hence increased seed production potential. The knowledge of the genes and genetic pathways underpinning Q-related traits enhances our understanding of wheat domestication and wheat improvement.