New Honorary Member of the BSPP

Abstract

Jonathan D. G. Jones grew up in London and graduated in Botany from Cambridge University followed by graduate work at the PBI, Cambridge. His career in plant–microbe interactions began with Ausubel at Harvard, studying Rhizobium–legume associations. He then worked at Advanced Genetic Sciences Inc. where his expertise using broad host-range plasmids underpinned the development of plant genetic engineering tools using Agrobacterium. Since 1988, he has led a research team at The Sainsbury Lab (TSL), Norwich, where he isolated the tomato Cf-9 gene for resistance to the fungus Cladosporium fulvum. Cf-9 encodes a pioneer cell surface “receptor-like protein” immune receptor, with extracellular leucine-rich repeats (LRRs). He isolated six such genes, each recognizing different fungal virulence factors. These preceded the Nobel prize-winning discoveries of similar Toll-like receptors in animal innate immunity. He went on to characterize complex immune receptor-encoding haplotypes with multiple paralogs and infer their evolutionary trajectories. He discovered that solvent-exposed amino acids in plant immune receptor LRRs are hypervariable and under diversifying selection for specific recognition of distinct pathogen molecules, and that unequal crossing over between paralogous genes at complex loci also contributes to receptor diversification. In a Cf-2 resistance gene suppressor screen, he discovered Rcr3, a cysteine protease required for Cf-2 to recognize the Avr2. In collaboration with the de Wit laboratory in Wageningen, he showed that Cf-2 “guards” Rcr3, activating defence when Rcr3 is inhibited by the Avr2 protease inhibitor. The resulting guard hypothesis was the subject of an influential paper with Dangl in 2001. He also identified several protein kinases and E3 ubiquitin ligases involved in Cf-dependent immunity, verifying their requirement for defence activation, and was first to show the role of receptor-like cytoplasmic kinases in cell surface receptor-mediated immunity. Most plant resistance genes encode intracellular nucleotide-binding LRR (NLR) immune receptors. He cloned one of the earliest (RPP5) and has defined >12 more. He was first to reveal the extreme haplotype diversity at the RPP5 locus between Arabidopsis accessions, again verifying extreme diversity in solvent-exposed amino acids of the LRRs of different paralogs, and unequal crossovers between paralogs in their evolution. In an influential 2006 paper with Dangl, he articulated the roles of cell surface “pattern-triggered immunity” and intracellular “effector-triggered immunity” in plant defence, integrating them for the first time. He has led discoveries on cross-talk between various hormone signalling pathways, in pathogen effector mechanisms, and in the role of variation in detection capacity in population resistance to disease. Some NLR receptors carry integrated domains (IDs) and are encoded adjacent in the genome to another NLR gene. Arabidopsis RPS4 and RRS1 are a paradigmatic example; RRS1 carries a WRKY transcription factor domain and the pair creates an immune receptor that detects pathogen effectors that act on WRKY domains. His work provided the first demonstration that NLRs can evolve to be immune receptors that contain IDs that mimic authentic pathogen targets. His fascination with genetic variation in host–pathogen interactions led him to develop sequence capture-based methods to interrogate plant immune receptor diversity. Resistance gene enrichment sequencing (RenSeq) has greatly accelerated our understanding of plant immune receptor repertoires. He also developed capture-based methods to investigate the genetic diversity of obligate parasites growing on hosts (PenSeq). He used RenSeq to address nonhost resistance (NHR) and defined the genetic basis of Arabidopsis NHR to Brassica-infecting races of white rust, revealing the crucial role of NLR receptors. Solanum americanum shows NHR to the potato late blight pathogen Phytophthora infestans. By isolating two NLR immune receptors, Rpi-amr1 and Rpi-amr3, from S. americanum, defining their recognized effectors from P. infestans, and verifying the efficacy of Rpi-amr1, Rpi-amr3, and Rpi-vnt1 in transgenic potato field experiments, he showed that their deployment might enable NHR to control blight in the field. He has played a key role in making the case that this approach to controlling crop disease is useful, safe, and sustainable. His discoveries in plant molecular genetics earned him election as Professor at UEA (1996), EMBO member (1998), Royal Society Fellow (2003), and International Member of US National Academy of Sciences (2015). He served in Royal Society working groups on food security and coauthored the Royal Society’s 2009 “Reaping the Benefits” report.