Maize metacaspases modulate the defense response mediated by the NLR protein Rp1-D21 likely by affecting its subcellular localization

Authors: LUAN, QING-LING - Shandong University; ZHU, YU-XIU - Shandong University; SUN, YANG - Shandong University; LIU, XIAO-YING - Shandong University; Balint-Kurti, Peter; LIU, MENGJIE - Shandong University; WANG, GUAN-FENG - Shandong University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/10/2020
Publication Date: 10/27/2020
Citation: Luan, Q., Zhu, Y., Sun, Y., Liu, X., Balint Kurti, P.J., Liu, M., Wang, G. 2020. Maize metacaspases modulate the defense response mediated by the NLR protein Rp1-D21 likely by affecting its subcellular localization. Plant Physiology. https://doi.org/10.1111/tpj.15047.
DOI: https://doi.org/10.1111/tpj.15047

Interpretive Summary: Metacaspases are plant proteins which are believed to be important in programed cell death and in disease resistance. We identified several maize metacaspases which interact with and modulate the effects of a plant disease resistance protein. It appeared that they did this by changing the subcellular localization of the resistance protein.

Technical Abstract: Plants usually employ resistance (R) genes to defend against pathogen infection, and most R genes encode nucleotide binding, leucine-rich-repeat (NLR) proteins. The recognition between R proteins and their cognate pathogens often triggers a hypersensitive response (HR), a rapid localized cell death at the site of pathogen infection. Metacaspases (MCs) belong to a family of cysteine proteases that are structurally related to metazoan caspases. MCs play important roles in plant innate immunity. However, the underlying molecular mechanism and the relationship between MC and NLR-mediated HR are not known. In this study, we systematically investigated the MC gene family in maize and identified 11 ZmMCs members belonging to two types. Further functional analysis showed that type I ZmMC1 and ZmMC2, but not type II ZmMC9 suppress the HR-inducting activity of the autoactive NLR protein Rp1-D21- and of its signaling domain CCD21-when transiently expressed in N. benthamiana. ZmMC1 and ZmMC2 physically associate with CCD21 in vivo. We further showed that ZmMC1 and ZmMC2, but not ZmMC9 are predominantly localized in a punctate distribution in both N. benthamiana and maize protoplast, and this punctate distribution seems to co-localize with the distribution of proteins associated with autophagy. Furthermore, the co-expression of ZmMC1 and ZmMC2 with Rp1-D21 and CCD21 cause their re-distribution from being uniformly distributed in the nucleocytoplasm to a punctate distribution co-localizing with ZmMC1 and ZmMC2. We reveal a novel role of plant MCs in modulating NLR-mediated defense response and derive a model to explain it.