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

<i>Phytophthora cinnamomi</i> Rands devastates forest species worldwide, causing significant ecological and economic impacts. The European chestnut (<i>Castanea sativa</i>) is susceptible to this hemibiotrophic oomycete, whereas the Asian chestnuts (<i>Castanea crenata</i> and <i>Castanea mollissima</i>) 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 <i>C. sativa</i> and <i>C. crenata</i> roots inoculated with <i>P. cinnamomi.</i> The studied time points represent the pathogen's hemibiotrophic lifestyle previously described at the cellular level. <i>Phytophthora cinnamomi</i> 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 (<i>elicitins</i> and <i>NLPs</i>) and sporulation-related genes was higher in the susceptible chestnut. After pathogen inoculation, 1,556 and 488 genes were differentially expressed by <i>C. crenata</i> and <i>C. sativa</i>, respectively. The most significant transcriptional changes occur at 2 h after inoculation (hai) in <i>C. sativa</i> and 48 hai in <i>C. crenata</i>. Nevertheless, <i>C. crenata</i> induced more defense-related genes, indicating that the resistant response to <i>P. cinnamomi</i> 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 <i>C. crenata</i>. Collectively, this study provides a comprehensive time-resolved description of the chestnut-<i>P. cinnamomi</i> dynamic, revealing new insights into susceptible and resistant host responses and important pathogen strategies involved in disease development.