NBS-LRR Protein Pik-H4 Interacts with OsBIHD1 to Balance Rice Blast Resistance and Growth by Coordinating Ethylene-Brassinosteroid Pathway

Abstract

The regulation of innate immunity and plant growth, along with the trade-off between them, affects the defense and recovery mechanisms of the plant after it is attacked by pathogens. Although it is known that hormonal crosstalk plays a major role in regulating interaction of plant growth and PAMP-triggered immunity, the relationship between plant growth and effector-triggered immunity (ETI) remains unclear. In a large-scale yeast two-hybrid screening for Pik-H4-interacting proteins, a homeodomain transcription factor OsBIHD1 was identified, which is previously known to function in biotic and abiotic stress responses. The knockout of OsBIHD1 in rice lines carrying Pik-H4 largely compromised the resistance of the rice lines to Magnaporthe oryzae, the fungus that causes rice blast. While overexpression of OsBIHD1 resulted in enhanced expression of the pathogenesis-related (PR) and ethylene (ET) synthesis genes. Moreover, OsBIHD1 was also found to directly bind to the promoter region of ethylene-synthesis enzyme OsACO3. In addition, OsBIHD1 overexpression or deficiency provoked dwarfism and reduced brassinosteroid (BR) insensitivity through repressing the expression of several critical genes involved in BR biosynthesis and BR signaling. During M. oryzae infection, transcript levels of the crucial BR catabolic genes (CYP734A2, CYP734A4, and CYP734A6) were significantly up-regulated in OsBIHD1-OX plants. Furthermore, OsBIHD1 was found to be capable of binding to the sequence-specific cis-elements on the promoters of CYP734A2 to suppress the plant growth under fungal invasion. Our results collectively suggest a model that OsBIHD1 is required for Pik-H4-mediated blast resistance through modulating the trade-off between resistance and growth by coordinating brassinosteroid-ethylene pathway.

Heterologous Expression of the Cotton NBS-LRR Gene GbaNA1 Enhances Verticillium Wilt Resistance in Arabidopsis

“…Identification of effective Verticillium wilt resistance genes is difficult because of the complexity of the cotton genome and aggressive pathogenicity of V. dahliae on most cultivars, although at least 80 different Verticillium wilt resistance quantitative trait loci (QTLs) have been reported on cotton ( Wang et al, 2007 , 2008 , 2012 ; Yang et al, 2008 ; Jiang et al, 2009 ; Zhao et al, 2014 ). At present, the homology-based cloning or differential expression screening are generally employed to clone Verticillium wilt resistance genes, and several genes have been identified and proven to play important roles during V. dahliae infection on cotton ( Munis et al, 2010 ; Gao et al, 2013 ; Zhang et al, 2013b ; Zhao et al, 2013 ; Mo et al, 2015 ; Duan et al, 2016 ; Li et al, 2016 ; Yang et al, 2016 ; Gong et al, 2017 ; Liu H. et al, 2017 ). However, only a few of these have the R gene characteristics.…”

“…The overexpression of VaRGA1 in Nicotiana benthamiana conferred enhanced resistance to Phytophthora parasitica through the activation of salicylic acid (SA) signaling and phenylpropanoid pathways ( Li X. et al, 2017 ). In cotton, defense responses including hormone signaling, ROS scavenging and activation of the pathogenesis-related gene expression, were all proven to play roles in Verticillium wilt resistance ( Gao et al, 2013 ; Zhang et al, 2013a ; Mo et al, 2015 ; Duan et al, 2016 ; Yang et al, 2016 ; Gong et al, 2017 ; Liu H. et al, 2017 ). The NBS-LRR protein GbaNA1 can be significantly induced following treatment with the ethylene ( Li N.Y. et al, 2017 ), and several genes encoding ethylene-responsive element-binding factor were significantly up-regulated after GbaNA1 overexpression in A. thaliana .…”

“…The resistance genes activate diverse defense responses following infection by V. dahliae , including the regulation of defense hormone (salicylic acid, ethylene, etc.) levels that are involved in spermine and camalexin signaling, enhancing reactive oxygen species scavenging capacity and oxidative stress tolerance, activating the expression of the pathogenesis-related genes, and accelerating phytoalexin (gossypol) synthesis ( Gao et al, 2013 ; Zhang et al, 2013a ; Mo et al, 2015 ; Duan et al, 2016 ; Yang et al, 2016 ; Gong et al, 2017 ; Liu H. et al, 2017 ). For instance, silencing of GbNRX1 , a thioredoxin, resulted in defective dissipation of apoplastic ROS, which led to higher ROS accumulation within protoplasts and hence critical for the apoplastic immune response ( Li et al, 2016 ).…”

Gaining Insight into Exclusive and Common Transcriptomic Features Linked with Biotic Stress Responses in Malus

“…A homeodomain transcription factor OsBIHD1 is known to be involved in biotic and abiotic stress responses. The overexpression of this gene or its deficiency modulated the expression of several brassinosteroid-related genes causing brassinosteroid insensitivity (Liu et al, 2017 ). Indeed the function of this gene seems to modulate the trade-off between resistance and growth by regulating brassinosteroid-ethylene pathway (Liu et al, 2017 ).…”

“…The overexpression of this gene or its deficiency modulated the expression of several brassinosteroid-related genes causing brassinosteroid insensitivity (Liu et al, 2017 ). Indeed the function of this gene seems to modulate the trade-off between resistance and growth by regulating brassinosteroid-ethylene pathway (Liu et al, 2017 ). In addition it is worthy to notice that a squalene monoxygenase and squalene epoxidase3 were induced exclusively by Pythium infections among the 13 analyzed studies.…”