Differing Responses to Phytophthora cinnamomi Infection in Susceptible and Partially Resistant Persea americana (Mill.) Rootstocks: A Case for the Role of Receptor-Like Kinases and Apoplastic Proteases

Abstract

The hemibiotrophic plant pathogen Phytophthora cinnamomi Rands is the most devastating pathogen of avocado (Persea americana Mill.) and, as such, causes significant annual losses in the industry. Although the molecular basis of P. cinnamomi resistance in avocado and P. cinnamomi virulence determinants have been the subject of recent research, none have yet attempted to compare the transcriptomic responses of both pathogen and host during their interaction. In the current study, the transcriptomes of both avocado and P. cinnamomi were explored by dual RNA sequencing. The basis for partial resistance was sought by the inclusion of both susceptible (R0.12) and partially resistant (Dusa®) rootstocks sampled at early (6, 12 and 24 hours post-inoculation, hpi) and late time-points (120 hpi). Substantial differences were noted in the number of differentially expressed genes found in Dusa® and R0.12, specifically at 12 and 24 hpi. Here, the partially resistant rootstock perpetuated defense responses initiated at 6 hpi, while the susceptible rootstock abruptly reversed course. Instead, gene ontology enrichment confirmed that R0.12 activated pathways related to growth and development, essentially rendering its response at 12 and 24 hpi no different from that of the mock-inoculated controls. As expected, several classes of P. cinnamomi effector genes were differentially expressed in both Dusa® and R0.12. However, their expression differed between rootstocks, indicating that P. cinnamomi might alter the expression of its effector arsenal based on the rootstock. Based on some of the observed differences, several P. cinnamomi effectors were highlighted as potential candidates for further research. Similarly, the receptor-like kinase (RLK) and apoplastic protease coding genes in avocado were investigated, focusing on their potential role in differing rootstock responses. This study suggests that the basis of partial resistance in Dusa® is predicated on its ability to respond appropriately during the early stages following P. cinnamomi inoculation, and that important components of the first line of inducible defense, apoplastic proteases and RLKs, are likely to be important to the observed outcome.

The expression of the NPR1-dependent defense response pathway genes in Persea americana (Mill.) following infection with Phytophthora cinnamomi

“…Downregulation of PaNPR5 was signi cant in both Dusa® and R0.12 at 6 hpi and persisted in Dusa® at 12 and 24 hpi, but not R0.12. Moreover, previous analyses of the data utilized in this study indicated that genes related to growth and developmental pathways were downregulated at 12 and 24 hpi in Dusa®, but not R0.12 [90]. This not only adds support to the putative developmental role of PaNPR5 but to the disparity in the duration of the initial defense responses between Dusa® and R0.12, as growth and defense are generally considered antithetical processes.…”

“…Whereas 72% and 80% mapped back in the P. cinnamomi inoculated R0.12 and Dusa® samples. A complete report for the data included in this study was recently published [90].…”

Comparative transcriptional analysis of Persea americana MYB, WRKY and AP2/ERF transcription factors following Phytophthora cinnamomi infection

“…SAR would prime defence responses away from infection sites to prepare cells for future infection. This would explain why the expression levels of PRR genes, which encode receptor-like kinases, increase at 120 hpi in both rootstocks, as reported by Backer et al (2022). A higher abundance of these receptors in uninfected cells would lead to stronger immune response activation once infection does occur (Andam et al, 2020;Palaniyandi & Muthuswamy, 2017).…”

“…Furthermore, these expression patterns may explain the differences in callose deposition, PRR and NLR expression patterns previously observed within resistant and susceptible rootstocks following P. cinnamomi infection (Backer et al, 2022;Fick, Swart, Backer, et al, 2022;van den Berg et al, 2018). Because plant-pathogen interactions are extremely complex, the cause of these observations can only be hypothesized.…”

Identification of Phytophthora cinnamomi CRN effectors and their roles in manipulating cell death during Persea americana infection

“…The expression data of 25 PcinCRN effectors were obtained by previously generated dual RNA-seq data of susceptible (R0.12) and partially resistant (Dusa®) P. americana rootstocks inoculated with P. cinnamomi GKB4 [ 50 ]. Briefly, RNA-seq reads were trimmed, and low-quality bases were removed using Trimmomatic v. 0.39 [ 51 ].…”