A fungal effector and a rice NLR protein have antagonistic effects on a Bowman–Birk trypsin inhibitor

Abstract

Bowman-Birk trypsin inhibitors (BBIs) play important roles in animal and plant immunity, but how these protease inhibitors are involved in the immune system remains unclear. Here, we show that the rice (Oryza sativa) BBI protein APIP4 is a common target of a fungal effector and an NLR receptor for innate immunity. APIP4 exhibited trypsin inhibitor activity in vitro and in vivo. Knockout of APIP4 in rice enhanced susceptibility, and overexpression of APIP4 increased resistance to the fungal pathogen Magnaporthe oryzae. The M. oryzae effector AvrPiz-t interacted with APIP4 and suppressed APIP4 trypsin inhibitor activity. By contrast, the rice NLR protein Piz-t interacted with APIP4, enhancing APIP4 transcript and protein levels, and protease inhibitor activity. Our findings reveal a novel host defence mechanism in which a host protease inhibitor targeted by a fungal pathogen is protected by an NLR receptor.

Weighted Gene Co-Expression Network Coupled with a Critical-Time-Point Analysis during Pathogenesis for Predicting the Molecular Mechanism Underlying Blast Resistance in Rice

“…This research reveals that many genes are involved in the defense network of Piz-t-KJ201, consistent with previous observations (Park et al 2012(Park et al , 2016Wang et al 2019;Bai et al 2019;Zhang et al 2020). These genes and TFs identified in the present study were of high biological relevance.…”

“…In our earlier studies, four proteins of a receptor-like protein kinase (gi|59,800,021), a NADP dependent malic enzyme (gi|54,606,800), a putative transaldolase (gi|57, 900,129), and a putative bowman birk trypsin inhibitor (gi|53,792,234), three C3HC4-type Ring finger E3 ubiquitin ligase (APIP2, 6, 10), and a bowman-Birk type bran trypsin inhibitor (APIP4) were confirmed to be involved in Piz-t-KJ201 interaction (Park et al 2012(Park et al , 2016Tian et al 2018;Zhang et al 2020). In the present study, we observed that a receptor-like protein kinase precursor (LOC_Os10g33040), a NADP-dependent malic enzyme (LOC_Os05g09440), a transaldolase (LOC_ Os08g05830), a bowman-Birk type bran trypsin inhibitor precursor (LOC_Os01g03360), and two zinc finger C3HC4 type domain containing protein (LOC_ Os01g20910 and LOC_Os12g04590) were also differentially regulated in Piz-t-KJ201 (Additional Table 2).…”

“…This gene was once widely used in breeding programs for increasing resistance to M. oryzae (Zhou et al 2006;Tian et al 2020). Numerous studies also have examined the interaction profiles of Piz-t-AvrPiz-t in rice (Park et al 2012(Park et al , 2016Wang et al 2016;Tang et al 2017;Tian et al 2018;Bai et al 2019;Zhang et al 2020). However, transcriptome profiling underlying the Piz-t-mediated rice resistance to blast fungus remains largely unknown.…”

Bowman-Birk Inhibitors: Insights into Family of Multifunctional Proteins and Peptides with Potential Therapeutical Applications

“…The effector is recognized by the cognate host resistance protein Piz-t; however, these two proteins do not interact directly. Zhang et al [220] showed that the rice (Oryza sativa) BBI protein, named APIP4 (AvrPiz-t interacting protein 4), was involved in this interaction and played a positive role in rice immunity. The fungal AvrPiz-t directly targets APIP4 and reduces its inhibitor activity in vivo and in vitro.…”

Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.)

“…Oryzae [26]. One rice BBI, APIP4, interacts at the protein level with both a fungal effector and host NLR receptors as part of the innate immune response, and plants carrying lossof-function mutations in this gene exhibit increased susceptibility to Magnaporthe oryzae [27]. In wheat, genetic mapping studies identi ed putative BBI genes as candidates for seedling resistance to tan spot [28] and Fusarium head blight [29].…”