An epiphany for plant resistance proteins and its impact on calcium‐based immune signalling

Abstract

Flor first postulated the gene-for-gene hypothesis in 1942, which states that 'for each (Resistance, R) gene that conditions reaction in the host there is a corresponding (Avirulence, avr) gene in the parasite that conditions pathogenicity' (Flor, 1971). This is, in fact, the so-called effector-triggered immunity (ETI) described in the 'Zig-Zag model ' (proposed in 2006), which describes alternating phases of immunity during the attempted infection of plants (Ngou et al., 2022). The initial phase, pattern-triggered immunity (PTI), is activated after the sensing of conserved 'patterns' (typically of microbial origin, but they can also be secondary plant-derived signals from damaged tissues) at the cell surface by membrane-localized pattern recognition receptors (PRRs). Adapted pathogens secrete PTI-dampening effector molecules to infect plants, but during evolution, resistant plants may acquire effector detection mechanisms that ultimately lead to ETI, a defence response of higher amplitude than PTI. Retrospectively, Flor's avirulence factors are the effectors secreted by pathogens, but they (or their effects) can be counteracted by R proteins. Understandably, breeders have been keen to identify R genes and develop them to generate disease resistant crops. Starting with the first in 1992, hundreds of R genes have now been cloned, the majority of which encode proteins with conserved structural motifs, termed nucleotide-binding leucine-rich repeat receptors (NLRs). These are further subdivided into CNLs or TNLs that possess either an N-terminal coiled-coil (CC) or a Toll-Interleukin-1 Receptor (TIR) domain, respectively (Kourelis & van der Hoorn, 2018). CNLs are functionally self-sufficient for immune signalling, while TNLs require a special class of 'helper' CNLs called RNLs (due to their CC domain being first described in the R protein RPW8). Furthermore, studies have shown that genes for the membrane-associated protein NDR1 (Non race-specific Disease Resistance 1) and the lipase-like protein EDS1 (Enhanced Disease Susceptibility 1) are required for immune signalling by CNLs and TNLs, respectively (Ngou et al., 2022). However, our understanding of the molecular mechanisms relating to these NLR proteins has been limited. In this issue of New Phytologist, Kim et al. (2022; pp. 813-818) and Parker et al. (2022; pp. 819-826) review recent progress that has completely transformed our understanding of NLR biochemistryboth CNLs and TNLs ultimately converge on generating calcium-permeable pores in plant membranes. Hence, one can anticipate that calcium-based signalling will lead the next 'wave' of insights into signal transduction from plant resistance proteins.

What’s new in protein kinase/phosphatase signalling in the control of plant immunity?

“…Finally, does the calcium signalling generated by the NLR pores lead to the sustained MAPK activation typically seen for ETI and if so, are (and which) RLCKs involved to phosphorylate the MKKKs? These and additional questions have been posed recently [ 116 ] and await future clarifications from the plant immunity community.…”