Crop immunity against viruses: outcomes and future challenges

Abstract

Viruses cause epidemics on all major cultures of agronomic importance, representing a serious threat to global food security. As strict intracellular pathogens, they cannot be controlled chemically and prophylactic measures consist mainly in the destruction of infected plants and excessive pesticide applications to limit the population of vector organisms. A powerful alternative frequently employed in agriculture relies on the use of crop genetic resistances, approach that depends on mechanisms governing plant-virus interactions. Hence, knowledge related to the molecular bases of viral infections and crop resistances is key to face viral attacks in fields. Over the past 80 years, great advances have been made on our understanding of plant immunity against viruses. Although most of the known natural resistance genes have long been dominant R genes (encoding NBS-LRR proteins), a vast number of crop recessive resistance genes were cloned in the last decade, emphasizing another evolutive strategy to block viruses. In addition, the discovery of RNA interference pathways highlighted a very efficient antiviral system targeting the infectious agent at the nucleic acid level. Insidiously, plant viruses evolve and often acquire the ability to overcome the resistances employed by breeders. The development of efficient and durable resistances able to withstand the extreme genetic plasticity of viruses therefore represents a major challenge for the coming years. This review aims at describing some of the most devastating diseases caused by viruses on crops and summarizes current knowledge about plant-virus interactions, focusing on resistance mechanisms that prevent or limit viral infection in plants. In addition, I will discuss the current outcomes of the actions employed to control viral diseases in fields and the future investigations that need to be undertaken to develop sustainable broad-spectrum crop resistances against viruses.

Keywords: PAMP-triggered immunity; R gene; crop improvement; gene silencing; plant virus; recessive resistance; systemic acquired resistance.

FIGURE 1

Prophylactic measures and main crop improvement strategies employed to control plant viral diseases.

FIGURE 2

Known antiviral immune mechanisms in plants. Plant resistance mechanisms against viruses are complementary in terms of plant defense timing, location (from the first infected cell to the generalized colonization) and targeting the virus-derived molecules (genome or proteins from viruses). (A) NBS-LRR dominant resistance relies on the interaction between an avirulence factor and a specific R gene product, and is effective several days after the virus entry into the plant. The HR-associated phenomenon confines the viral pathogen in the infected and neighboring cells. (B) Recessive resistance, that corresponds to the absence of appropriate host factors that are required for the virus cycle, is a non-inducible resistance, passive and effective throughout plant colonization. It confers resistance at the infection step that requires the cellular factor of interest.(C) RNA interference (RNAi) targets viral nucleic acids. Once set up after few days, the effectiveness of this defense mechanism increases and spreads to the whole plant through a relay-amplification process. (D) Hormone-mediated resistance against viral pathogens is represented here by the role of salicylic acid (SA) and methyl-salicylate (Me-SA) in systemic acquired resistance (SAR). On graphs, R, resistance level; t, infection timing.

FIGURE 3

Plant innate immunity vs. Plant adaptive immunity. Following entry into a host cell and genome decapsidation, the virus genome is liberated and replicated, leading to the accumulation of pathogenic nucleic acids that are perceived as viral PAMPs by specific intracellular PRRs. This recognition triggers a downstream cascade leading to PTI responses. Virus genome translation (occurring simultaneous to replication) leads to the synthesis of the virus-encoded proteins, among which viral pathogenic effectors enable the suppression of PTI signaling. In turn, specific plant R genes interact (directly or indirectly) with these effectors (that are then called avirulence factors) to trigger ETI. In the case of plant adaptive immunity illustrated by RNA interference (RNAi), the virus-derived elicitor molecules, corresponding to replicative dsRNAs or structured (str-RNA) viral genomes, are recognized by DCLs, key component of the silencing machinery that leads to virus degradation at the nucleic acid level. Viral proteins acting as RNAi-suppressing effectors interfere with this defense pathway. A recent publication (Sansregret et al., 2013) suggests silencing suppressors may be targeted by ETI-like mechanisms, restoring plant resistance. The main steps of the virus cycle into the first infected cell have been mentioned into gray boxes.