Adam D. Steinbrenner, Maria Muñoz-Amatriaín, Antonio F. Chaparro, Jessica Montserrat Aguilar-Venegas, Sassoum Lo, Satohiro Okuda, Gaetan Glauser, Julien Dongiovanni, Da Shi, Marlo Hall, Daniel Crubaugh, Nicholas Holton, Cyril Zipfel, Ruben Abagyan, Ted C. J. Turlings, Timothy J. Close, Alisa Huffaker, and Eric A. Schmelz

PNAS December 8, 2020 117 (49) 31510-31518

Significance

Plants respond to biotic attack using an immune system of receptors to recognize molecules associated with danger. We identified an immune receptor, termed inceptin receptor (INR), able to confer responses to defined inceptin peptide fragments present in caterpillar oral secretions. Like many plant immune receptors, INR is encoded only by certain plant species but can be transferred across families to confer new signaling and defense functions. While INR is only found in the genomes of cowpea, common bean, and related legumes, it confers defined elicitor responses to transgenic tobacco and suppresses the growth of attacking beet armyworm larvae. INR expands the breadth of plant pattern recognition receptors to detection of chewing insect herbivores.

Abstract

Herbivory is fundamental to the regulation of both global food webs and the extent of agricultural crop losses. Induced plant responses to herbivores promote resistance and often involve the perception of specific herbivore-associated molecular patterns (HAMPs); however, precisely defined receptors and elicitors associated with herbivore recognition remain elusive. Here, we show that a receptor confers signaling and defense outputs in response to a defined HAMP common in caterpillar oral secretions (OS). Staple food crops, including cowpea (Vigna unguiculata) and common bean (Phaseolus vulgaris), specifically respond to OS via recognition of proteolytic fragments of chloroplastic ATP synthase, termed inceptins. Using forward-genetic mapping of inceptin-induced plant responses, we identified a corresponding leucine-rich repeat receptor, termed INR, specific to select legume species and sufficient to confer inceptin-induced responses and enhanced defense against armyworms (Spodoptera exigua) in tobacco. Our results support the role of plant immune receptors in the perception of chewing herbivores and defense.

See: https://www.pnas.org/content/117/49/31510

Figure 1: Cowpea responses to an inceptin peptide associate with a single genetic locus. (A) Ethylene production in cowpea accessions after treatment with H₂O or 1 μM inceptin peptides. Bars show means ± SEM of replicate leaflets for individual inceptin treatments (n = 3) and all combined respective H₂O controls with label “All” (n = 21). Different letters represent significant differences (All ANOVAs P < 0.05; Tukey honestly significant difference [HSD], α = 0.05). (B) QTL statistics for ethylene production ratio, Vu-In^-A/H₂O, in the Yacine × 58-77 RIL population. The dotted line indicates false discovery rate (FDR) significance cutoff (17,638 SNPs; modified Bonferroni correction at α = 0.05) (C) Manhattan plot of GWAS results for ethylene production ratio, Vu-In^-A/H₂O, in 364 cowpea Minicore accessions. The dotted line indicates FDR cutoff at α = 0.05 for 42,686 SNPs assigned respective physical coordinates in the cowpea genome (19). (D) Genomic region of chromosome 7 (Vu07; positions 34,220,090 to 34,258,839) containing highly associated marker SNPs (2_22560/1) and syntenic genes on common bean chromosome 7. Green and black filled arrows indicate LRR-RLP encoding genes.