Reducing brassinosteroid signaling enhances grain yield in semi-dwarf wheat

Authors: SONG, LONG - China Agricultural University; LIU, JIE - China Agricultural University; CAO, BEILU - China Agricultural University; LIU, BIN - China Agricultural University; ZHANG, XIAOPING - China Agricultural University; CHEN, ZHAOYAN - China Agricultural University; DONG, CHAOQUN - China Agricultural University; LIU, XIAOQING - China Agricultural University; ZHANG, ZHAOHENG - China Agricultural University; WANG, WENXI - China Agricultural University; CHAI, LINGLING - China Agricultural University; LIU, JING - China Agricultural University; ZHU, JUN - China Agricultural University; CUI, SHUBIN - China Agricultural University; HE, FEI - China Agricultural University; PENG, HUIRU - China Agricultural University; HU, ZHAORONG - China Agricultural University; SU, ZHENQI - China Agricultural University; GUO, WEILONG - China Agricultural University; XIN, MINGMING - China Agricultural University; YAO, YINGYIN - China Agricultural University; YAN, YONG - China Agricultural University; SONG, YINMING - China Agricultural University; Bai, Guihua; SUN, QIXIN - China Agricultural University; NI, ZHONGFU - China Agricultural University

Submitted to: Nature
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/27/2023
Publication Date: 4/26/2023
Citation: Song, L., Liu, J., Cao, B., Liu, B., Zhang, X., Chen, Z., Dong, C., Liu, X., Zhang, Z., Wang, W., Chai, L., Liu, J., Zhu, J., Cui, S., He, F., Peng, H., Hu, Z., Su, Z., Guo, W., Xin, M., Yao, Y., Yan, Y., Song, Y., Bai, G., Sun, Q., Ni, Z. 2023. Reducing brassinosteroid signaling enhances grain yield in semi-dwarf wheat. Nature. 617:118-124. https://doi.org/10.1038/s41586-023-06023-6.
DOI: https://doi.org/10.1038/s41586-023-06023-6

Interpretive Summary: Modern wheat cultivars usually carry either Rht-B1b or Rht-D1b semi-dwarfing genes to reduce plant height and thus reduce lodging. However, the two genes also reduce nitrogen-use efficiency, produce smaller grains, and require higher nitrogen inputs to maintain their grain yields. We discovered that a wheat variety missing the genes Rht-B1b and ZnF-B due to a natural mutation also had reduced plant height, but with more compact plant architecture and higher grain yield in the field trials. We found that deletion of ZnF-B induced the semi-dwarf trait by attenuating brassinosteroid perception and deletion of Rht-B1 improved yield traits. Our findings provide a creative strategy to design high-yield semi-dwarf wheat varieties by manipulating brassinosteriod signaling pathway to increase wheat production.

Technical Abstract: Modern ‘Green Revolution’ wheat varieties (GRVs) confer semi-dwarf and lodging-resistant plant architecture owing to the Reduced height-B1b (Rht-B1b) and Rht-D1b alleles1. However, both Rht-B1b and Rht-D1b are gain-of-function mutant alleles encoding gibberellin (GA) signaling repressors that stably repress plant growth and negatively affect nitrogen-use efficiency (NUE) and grain filling2–5. Therefore, the GRVs harboring Rht-B1b or Rht-D1b usually produce smaller grain and require higher nitrogen fertilizer inputs to maintain their grain yields. Here we describe a new strategy to design semi-dwarf wheat varieties without the need of Rht-B1b or Rht-D1b alleles. We discovered that missing of the Rht-B1 and ZnF-B (a RING-type E3 ligase) in a ~500 kb haploblock natural deletion shaped semi-dwarf plants with more compact plant architecture and substantially improved grain yield (up to 15.2%) in the field trials. Further genetic analysis confirmed that the deletion of ZnF-B induced the semi-dwarf trait in the absence of the Rht-B1b and Rht-D1b alleles through attenuating brassinosteroid (BR) perception. ZnF acts as a BR signaling activator to facilitate proteasomal destruction of BR signaling repressor BRI1 Kinase Inhibitor 1 (TaBKI1); whereas the loss of ZnF stabilizes TaBKI1 to block BR signaling transduction. Our findings not only identified a pivotal BR signaling modulator but also provided a creative strategy to design high-yield semi-dwarf wheat varieties by manipulating BR signal pathway to sustain wheat production.