Variation in microbial feature perception in the Rutaceae family with immune receptor conservation in citrus

Abstract

Although much is known about the responses of model plants to microbial features, we still lack an understanding of the extent of variation in immune perception across members of a plant family. In this work, we analyzed immune responses in Citrus and wild relatives, surveying 86 Rutaceae genotypes with differing leaf morphologies and disease resistances. We found that responses to microbial features vary both within and between members. Species in two subtribes, the Balsamocitrinae and Clauseninae, can recognize flagellin (flg22), cold shock protein (csp22) and chitin, including one feature from Candidatus Liberibacter species (csp22CLas), the bacterium associated with Huanglongbing. We investigated differences at the receptor level for the flagellin receptor FLAGELLIN SENSING 2 (FLS2) and the chitin receptor LYSIN MOTIF RECEPTOR KINASE 5 (LYK5) in citrus genotypes. We characterized two genetically linked FLS2 homologs from ‘Frost Lisbon’ lemon (Citrus ×limon, responsive) and ‘Washington navel’ orange (Citrus ×aurantium, non-responsive). Surprisingly, FLS2 homologs from responsive and non-responsive genotypes were expressed in Citrus and functional when transferred to a heterologous system. ‘Washington navel’ orange weakly responded to chitin, whereas ‘Tango’ mandarin (Citrus ×aurantium) exhibited a robust response. LYK5 alleles were identical or nearly identical between the two genotypes and complemented the Arabidopsis (Arabidopsis thaliana) lyk4/lyk5-2 mutant with respect to chitin perception. Collectively, our data indicate that differences in chitin and flg22 perception in these citrus genotypes are not the results of sequence polymorphisms at the receptor level. These findings shed light on the diversity of perception of microbial features and highlight genotypes capable of recognizing polymorphic pathogen features.

Natural variation of immune epitopes reveals intrabacterial antagonism

“…54 While CORE is restricted to the Solanaceae, other genotypes in the Vitaceae and Rutaceae families respond to csp22 variants. 10, 55 Considering CSP diversity, it is likely other convergently evolved PRRs recognize and respond to csp22 variants.…”

“…Each plant genome contains hundreds of candidate PRRs; thus, it is possible that linage specific, convergent evolved receptors is common and the broad conservation of FLS2 is the exception (54). While CORE is restricted to the Solanaceae, other genotypes in the Vitaceae and Rutaceae families respond to csp22 variants (10,55). Considering CSP diversity, it is likely other convergently evolved PRRs recognize and respond to csp22 variants.…”

“…6,7,8,9 FLS2, unlike most PRRs, is broadly found throughout the plant kingdom. 7,9,10 Since the flg22-FLS2 discovery, researchers have uncovered other bacterial epitope-receptor pairs specific to certain plant families. For instance, the Elongation Factor Tu derived epitope elf18 interacts with the EFR receptor, which is present in the Brassicaceae family.…”

“…The most well-studied PRR is FLAGELLIN-SENSING 2 (FLS2), which recognizes the 22-amino acid epitope, flg22, from bacterial flagellin FliC (6-9). Unlike most PRRs, FLS2 is conserved throughout the plant kingdom (7,9,10). Since the flg22-FLS2 discovery, researchers have uncovered other epitope-receptor pairs restricted to certain plant families.…”

Natural variation in the pattern‐triggered immunity response in plants: Investigations, implications and applications

“…In every case of which we are aware where this question has been addressed, significant variation has been identified. Variation in the PTI response between lines has been reported in tomatoes (Bhattarai et al., 2016 ; Roberts et al., 2019 ; Veluchamy et al., 2014 ), Arabidopsis (Vetter et al., 2012 , 2016 ), B. napus (Lloyd et al., 2014 ), citrus (Trinh et al., 2023 ), soybean (Valdes‐Lopez et al., 2011 ), maize (Wang et al., 2021 ; Zhang et al., 2017 ) and sorghum (Kimball et al., 2019 ; Samira et al., 2019 ; Tuleski et al., 2020 ). It therefore seems likely that this type of variation is the rule rather than the exception.…”