Functional modulation of an aquaporin to intensify photosynthesis and abrogate bacterial virulence in rice. (18th September 2021)

• Record Type: Journal Article
• Authors: Chen, Xiaochen; Ma, Jinbiao; Wang, Xuan; Lu, Kai; Liu, Yan; Zhang, Liyuan; Peng, Jinfeng; Chen, Lei; Yang, Minkai; Li, Yang; Cheng, Zaiquan; Xiao, Suqin; Yu, Jinfeng; Zou, Shenshen; Liang, Yuancun; Zhang, Meixiang; Yang, Yonghua; Ding, Xinhua; Dong, Hansong
• Is Part Of: Plant journal. Volume 108:Number 2(2021)
• Page Start: 330
• Page End: 346
• Publication Date: 2021-09-18
• Subjects: aquaporin -- OsPIP1;3 -- CO2 transport -- photosynthesis -- grain yield -- functional switch -- bacterial effectors -- translocation -- disease control; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15427
• Languages: English
• ISSNs: 0960-7412

Abstract

SUMMARY: Plant aquaporins are a recently noted biological resource with a great potential to improve crop growth and defense traits. Here, we report the functional modulation of the rice ( Oryza sativa ) aquaporin OsPIP1;3 to enhance rice photosynthesis and grain production and to control bacterial blight and leaf streak, the most devastating worldwide bacterial diseases in the crop. We characterize OsPIP1;3 as a physiologically relevant CO2 ‐transporting facilitator, which supports 30% of rice photosynthesis on average. This role is nullified by interaction of OsPIP1;3 with the bacterial protein Hpa1, an essential component of the Type III translocon that supports translocation of the bacterial Type III effectors PthXo1 and TALi into rice cells to induce leaf blight and streak, respectively. Hpa1 binding shifts OsPIP1;3 from CO2 transport to effector translocation, aggravates bacterial virulence, and blocks rice photosynthesis. On the contrary, the external application of isolated Hpa1 to rice plants effectively prevents OsPIP1;3 from interaction with Hpa1 secreted by the bacteria that are infecting the plants. Blockage of the OsPIP1;3–Hpa1 interaction reverts OsPIP1;3 from effector translocation to CO2 transport, abrogates bacterial virulence, and meanwhile induces defense responses in rice. These beneficial effects can combine to enhance photosynthesis by 29–30%, reduce bacterial disease by 58–75%, and increase grain yield by 11–34% in different rice varieties investigated in small‐scale field trials conducted during the past years. Our results suggest that crop productivity and immunity can be coordinated by modulating the physiological and pathological functions of a single aquaporin to break the growth–defense tradeoff barrier. Significance Statement: In rice ( Oryza sativa ), the aquaporin OsPIP1;3 usually facilitates cellular uptake of atmospheric CO2 to promote photosynthesis, but infection by Xanthomonas oryzae bacteria compels OsPIP1;3 to translocate the bacterial Type III (T3) effectors into the cytoplasm to cause leaf blight and streak. A technical approach designated as T3 Effector Translocation Interference (T3ETI) has been established to effectively control the bacterial diseases and enhance rice photosynthesis and grain production in small‐scale field trials. OsPIP1;3 facilitates cellular uptake of atmospheric CO2 to promote photosynthesis in rice plants without bacterial infection. Infection by Xanthomonas oryzae shifts OsPIP1;3 from CO2 transport to translocation of the bacterial Type III (T3) effectors into rice cells to cause leaf blight and streak. The functional switch is triggered by interaction of OsPIP1;3 with the bacterial protein Hpa1, which is an essential constituent of the T3 translocon. T3 Effector Translocation Interference (T3ETI) by blocking the OsPIP1;3–Hpa1 interaction controls both diseases and enhances rice photosynthesis and grain production.