Novel insights into the role of complex subcellular bodies regulating host-pathogen interactions.

Abstract

Food security and safety are an urgent concern with an ever-increasing human population and demands for healthier lives. Over the past 30 years, knowledge of how plants defend against pathogen infection has greatly helped in meeting these challenges. Many disease-resistance genes have been introduced into economically important crops, and new agricultural managements developed and deployed based on the understanding of the mechanisms of plant disease resistance. These advances have also significantly reduced the use of chemical pesticides to help protect our environment from further pollution and to mitigate climate change. However, many basic questions about the plant immune system and related subcellular bodies remain to be answered. Excitingly, fresh new insight has been achieved in several areas of plant–microbe interactions in the past several years. Groundbreaking discoveries, including cross-kingdom RNA, the exosome, and the resistome, for example, are revealing the crucial roles of complex subcellular bodies in the plant defence system, which has substantially elevated our understanding of plant disease resistance. In this Special Issue, we present a selection of papers to highlight recent advances in addressing these key areas in host–pathogen interactions. Cross-kingdom small RNA (sRNA) interference is a key discovery in recent years. sRNA interference is a well-known strategy for hosts to defend against viral pathogen infection. Many bacterial and fungal pathogens colonize and proliferate in the plant apoplastic niche, therefore how host sRNA can specifically target pathogen genes and how the sRNAs can travel between host and pathogen are the two major challenging questions. Extracellular vesicles (EVs) are the likely candidates in transporting small interfering RNAs (siRNAs). It is known that EVs act as shuttles and carry diverse cargos loaded with siRNAs, secreted proteins, defence proteins, and probably other small molecules. Intercellular/organismal communication using EVs is an intrinsic characteristic of life. Indeed, EVs are also found to transport defence materials from host to pathogens. Zhou et al. (pages 760–771) summarize the roles of EVs in plant–pathogen interactions with particular attention to sRNAs and defensive proteins in plant EVs. Since the gene-for-gene hypothesis was proposed 30 years ago, many pathogen-secreted effectors and the cognate plant resistance genes (typically encoding nucleotide-binding leucine-rich repeat [NLR] proteins) have been discovered. These discoveries have markedly increased our understanding of the plant immune system and enabled breeding for disease resistance. Despite these advances, knowledge of how NRL protfeins are activated and implement immunity has only recently come to light, with the first plant resistome (a concept adopted from animal immunity) structure being resolved in 2019. Liu and Wan (pages 772–780) provide a timely review on recent breakthroughs of the NLR protein-related resistome and the helper NLR proteins in this collection. In addition, other complex subcellular bodies are also integrally involved in disease resistance, although their functions have not been fully explored, for instance plasmodesmata and endoplasmic reticulum (ER). Iswanto et al. (pages 795–804) encapsulate recent advances in the study of pathogen effectors to target plant plasmodesmata associated with transportation and virulence. The research article by Liang et al. (pages 805–818) demonstrates that two factors of the ER-associated degradation machinery are activated by rice black-streaked dwarf virus to facilitate ER-to-cytosol export of ER tubules in Sogatella furcifera, the planthopper vector. This article highlights a novel role of ER functions in plant virus subcellular transport. Finally, a thoughtful review by Falter and Reumann (pages 781–794) from the pathogen side encapsulates pathogen peroxisomal functions in housing various enzymes for toxin production, melanization of appressoria, and other novel functions.