AUTHOR=Fernandes Patrícia , Pimentel Diana , Ramiro Ricardo S. , Silva Maria do Céu , Fevereiro Pedro , Costa Rita Lourenço 

TITLE=Dual transcriptomic analysis reveals early induced Castanea defense-related genes and Phytophthora cinnamomi effectors

JOURNAL=Frontiers in Plant Science

VOLUME=15

YEAR=2024

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2024.1439380

DOI=10.3389/fpls.2024.1439380

ISSN=1664-462X

ABSTRACT=<p><italic>Phytophthora cinnamomi</italic> Rands devastates forest species worldwide, causing significant ecological and economic impacts. The European chestnut (<italic>Castanea sativa</italic>) is susceptible to this hemibiotrophic oomycete, whereas the Asian chestnuts (<italic>Castanea crenata</italic> and <italic>Castanea mollissima</italic>) are resistant and have been successfully used as resistance donors in breeding programs. The molecular mechanisms underlying the different disease outcomes among chestnut species are a key foundation for developing science-based control strategies. However, these are still poorly understood. Dual RNA sequencing was performed in <italic>C. sativa</italic> and <italic>C. crenata</italic> roots inoculated with <italic>P. cinnamomi.</italic> The studied time points represent the pathogen’s hemibiotrophic lifestyle previously described at the cellular level. <italic>Phytophthora cinnamomi</italic> expressed several genes related to pathogenicity in both chestnut species, such as cell wall–degrading enzymes, host nutrient uptake transporters, and effectors. However, the expression of effectors related to the modulation of host programmed cell death (<italic>elicitins</italic> and <italic>NLPs</italic>) and sporulation-related genes was higher in the susceptible chestnut. After pathogen inoculation, 1,556 and 488 genes were differentially expressed by <italic>C. crenata</italic> and <italic>C. sativa</italic>, respectively. The most significant transcriptional changes occur at 2 h after inoculation (hai) in <italic>C. sativa</italic> and 48 hai in <italic>C. crenata</italic>. Nevertheless, <italic>C. crenata</italic> induced more defense-related genes, indicating that the resistant response to <italic>P. cinnamomi</italic> is controlled by multiple loci, including several pattern recognition receptors, genes involved in the phenylpropanoid, salicylic acid and ethylene/jasmonic acid pathways, and antifungal genes. Importantly, these results validate previously observed cellular responses for <italic>C. crenata</italic>. Collectively, this study provides a comprehensive time-resolved description of the chestnut–<italic>P. cinnamomi</italic> dynamic, revealing new insights into susceptible and resistant host responses and important pathogen strategies involved in disease development.</p>