Functional modulation of an aquaporin to intensify photosynthesis and abrogate bacterial virulence in rice

Abstract

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 CO 2 -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 CO 2 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 CO 2 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.

AtPIP1;4 and AtPIP2;4 Cooperatively Mediate H2O2 Transport to Regulate Plant Growth and Disease Resistance

“…Our study finds that AtPIP1;4 and AtPIP2;4 regulate plant growth, which is similar to earlier reports [51,52]. Some plant PIPs have been proven to be efficient CO 2 transport channels, capable of promoting CO 2 transport to enhance photosynthesis, thereby facilitating growth and grain yield [11,15,25]. We have also identified the important role of AtPIP1;4 in plant growth in our previous research, where AtPIP1;4 interacts with the Hpa1 to enhance CO 2 transport, net photosynthetic rate, and mesophyll conductance, thereby promoting plant growth [51].…”

“…AQPs are integral membrane proteins initially characterized as water (H 2 O) transport channels [12]. Subsequent studies have revealed that AQPs can also transport more than 20 small molecule compounds, such as CO 2 [11,[13][14][15], H 2 O 2 [9][10][11], NH 3 [16], NO [17], and others [18,19]. Through their function in mediating substrate transport, AQPs regulate a variety of pathological and physiological processes [4,[20][21][22].…”

“…In rice, OsPIP2;2 transports pathogen-induced H 2 O 2 into the cytoplasm and facilitates the translocation of the OsmaMYB into the nucleus, intensifying defense responses against pathogens [10]. OsPIP1;3 and OsPIP2;1 enhances rice growth and grain yield by facilitating CO 2 transport [15,25]. ZmPIP2;5 facilitates maize growth by transporting H 2 O [26][27][28].…”

“…The main structural distinctions between PIP1 and PIP2 lie in the lengths of their N-segment and C-terminal, and they also exhibit differences in their functional properties [32]. Several studies have indicated that certain PIP1 proteins have low efficiency in H 2 O transport [33,34], but they often acts as solute channels [15,35,36]. In comparison, the PIP2 group has been found to possess a higher capacity for H 2 O transport [37,38].…”

Comparative Transcript Profiling of Resistant and Susceptible Tea Plants in Response to Gray Blight Disease

“…Photosynthesis stands as a fundamental and universal process that is crucial for the survival of plants, while immune defense plays a pivotal role in adapting to the growth environment. Numerous studies have underscored the intricate interconnection between these two vital processes within a complex network [37][38][39][40][41]. Secondary metabolism pathways emerge as particularly crucial in tea plant resistance to diseases.…”