Date Published: September 8, 2016
Publisher: Public Library of Science
Author(s): Lian Jin, Qingqing Qin, Yu Wang, Yingying Pu, Lifang Liu, Xing Wen, Shaoyi Ji, Jianguo Wu, Chunhong Wei, Biao Ding, Yi Li, Savithramma P. Dinesh-Kumar.
The phytohormone auxin plays critical roles in regulating myriads of plant growth and developmental processes. Microbe infection can disturb auxin signaling resulting in defects in these processes, but the underlying mechanisms are poorly understood. Auxin signaling begins with perception of auxin by a transient co-receptor complex consisting of an F-box transport inhibitor response 1/auxin signaling F-box (TIR1/AFB) protein and an auxin/indole-3-acetic acid (Aux/IAA) protein. Auxin binding to the co-receptor triggers ubiquitination and 26S proteasome degradation of the Aux/IAA proteins, leading to subsequent events, including expression of auxin-responsive genes. Here we report that Rice dwarf virus (RDV), a devastating pathogen of rice, causes disease symptoms including dwarfing, increased tiller number and short crown roots in infected rice as a result of reduced sensitivity to auxin signaling. The RDV capsid protein P2 binds OsIAA10, blocking the interaction between OsIAA10 and OsTIR1 and inhibiting 26S proteasome-mediated OsIAA10 degradation. Transgenic rice plants overexpressing wild-type or a dominant-negative (degradation-resistant) mutant of OsIAA10 phenocopy RDV symptoms are more susceptible to RDV infection; however, knockdown of OsIAA10 enhances the resistance of rice to RDV infection. Our findings reveal a previously unknown mechanism of viral protein reprogramming of a key step in auxin signaling initiation that enhances viral infection and pathogenesis.
Viral infection causes enormous losses in crop yield and crop quality, posing a constant threat to food security. These losses are attributed to virus-induced abnormal growth and development, exhibited as disease symptoms. However, The molecular basis of disease symptom development in plants remains poorly understood [1–5]. Plant hormones control many aspects of the plant growth and development by orchestrating the expression of plant genes in a temporally and spatially regulated manner, and by coordinating plant responses to environmental cues. Perturbation of hormone signaling in plant often causes developmental defects, some of which share characteristics with virus-induced disease symptoms [2,6]. Viral infections also interfere with plant hormone homeostasis [6–10].
In the current study, we demonstrate a novel mechanism through which the initiation of auxin signaling pathways is reprogrammed by a viral protein, thereby causing morphogenesis alterations in rice and enhancing the viral infection (for a model, see Fig 7). Biochemically, this has evolved to be a highly specific process in which the RDV P2 protein interacts with OsIAA10, but not with other tested Aux/IAA proteins; and P2 binds domain II of OsIAA10, thereby inhibiting its interaction with SCFTIR1/AFBs and subsequent degradation that is key for the regulation of normal growth and development. Biologically, this reprogramming of auxin signaling initiation leads to the abnormal expression of rice genes that apparently benefit viral infection and enhance disease symptoms. The importance of this new mechanism, from a practical point of view and as demonstrated here, is that the engineered reduction of OsIAA10 can improve the resistance of rice to RDV infection. RDV-mediated alterations in the auxin signaling pathway are not just limited to OsIAA10, the mRNA expression of downstream genes with auxin response elements (AuxREs), including genes from the Aux/IAA, GH3, and SAUR families, were directly or indirectly affected by RDV infection (Fig 1E). However, OsIAA10 protein levels but not mRNA levels were changed upon RDV infection (Figs 1E, 3G, and S5 Fig).