Lessons in Effector and NLR Biology of Plant-Microbe Systems

Abstract

A diversity of plant-associated organisms secrete effectors-proteins and metabolites that modulate plant physiology to favor host infection and colonization. However, effectors can also activate plant immune receptors, notably nucleotide-binding domain and leucine-rich repeat region (NLR)-containing proteins, enabling plants to fight off invading organisms. This interplay between effectors, their host targets, and the matching immune receptors is shaped by intricate molecular mechanisms and exceptionally dynamic coevolution. In this article, we focus on three effectors, AVR-Pik, AVR-Pia, and AVR-Pii, from the rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae), and their corresponding rice NLR immune receptors, Pik, Pia, and Pii, to highlight general concepts of plant-microbe interactions. We draw 12 lessons in effector and NLR biology that have emerged from studying these three little effectors and are broadly applicable to other plant-microbe systems.

Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen

“…In plants, immune receptors of the NLR (nucleotide-binding, leucine-rich repeat) superfamily monitor the intracellular space for signatures of non-self, typically detecting translocated pathogen effector proteins either by direct-binding, or indirectly via monitoring their activity on host targets 3,4 . Co-evolution between pathogens and hosts has driven diversification of plant NLRs, with many NLR genes present in allelic series, with distinct effector recognition profiles [5][6][7][8][9][10][11][12][13][14][15] . Pathogen effectors can show strong signatures of positive selection including high levels of nonsynonymous (resulting in amino acid changes) over synonymous polymorphisms 5,7,12,[16][17][18] .…”

“…Genetically paired NLRs with integrated domains have repeatedly evolved in rice 29,30 , and can detect effectors from the rice blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae), the causative agent of the most devastating disease of rice -the staple crop that feeds more than half the world population 5,25,26,32 .…”

“…1a). Both the AVR-Pik effectors and the Pik NLRs exist as an allelic series in M. oryzae and rice respectively, most likely arisen through co-evolutionary dynamics between pathogen and host 5,34,35 . As such, they represent an excellent system for understanding the mechanistic basis of recognition in plant immunity.…”

CRISPR Crops: Plant Genome Editing Toward Disease Resistance

“…Pyricularia oryzae) (74). Remarkably, the Pi21 protein contains a heavy metal-associated (HMA) domain with similarity to domains targeted by the M. oryzae effectors AVR-Pik, AVR-Pia, and AVR-Co39 (24,40,148,169,243). S genes can also function as negative regulators of immune response and their impairment can lead to recessive resistance.…”

The roles of rice microRNAs in rice-Magnaporthe oryzae interaction

“…Virulent rice blast strains employ effectors, such as secreted LysM protein1 (Slp1), or avirulence genes, such as AVR-Pizt, to subvert PTI, leading to effector-triggered susceptibility (Mentlak et al 2012;Park et al 2016;Wang et al 2017). In turn, rice resistance (R) genes recognize avirulence effectors to activate the second layer of immunity, i.e., effector-triggered immunity (ETI), to contain the M. oryzae infection (Bialas et al 2018). To date, more than 30 R genes, most of which encode nucleotide-binding site leucine-rich repeat (NLR) family receptors, have been functionally characterized from rice, and nine associated cognate avirulence effectors from M. oryzae have been identified (Wang et al 2017;Xie et al 2019).…”