Validating alternative oxidase (AOX) gene family as efficient marker consortium for multiple-resilience in Xylella fastidiosa-infected Vitis holobionts.

AOX gene family in motion marks in-born efficiency of respiration adjustment; can serve for primer screening, genotype ranking, in vitro-plant discrimination and a SMART perspective for multiple-resilient plant holobiont selection. The bacteria Xylella fastidiosa (Xf) is a climate-dependent, global threat to many crops of high socio-economic value, including grapevine. Currently designed breeding strategies for Xf-tolerant or -resistant genotypes insufficiently address the danger of biodiversity loss by focusing on selected threats, neglecting future environmental conditions. Thus, breeding strategies should be validated across diverse populations and acknowledge temperature changes and drought by minimizing the metabolic-physiologic effects of multiple stress-induced oxygen shortages. This research hypothesizes that multiple-resilient plant holobionts achieve lifelong adaptive robustness through early molecular and metabolic responses in primary stress target cells, which facilitate efficient respiration adjustment and cell cycle down-regulation. To validate this concept open-access transcriptome data were analyzed of xylem tissues of Xf-tolerant and -resistant Vitis holobionts from diverse trials and genetic origins from early hours to longer periods after Xf-inoculation. The results indicated repetitive involvement of alternative oxidase (AOX) transcription in episodes of down-regulated transcripts of cytochrome c oxidase (COX) at various critical time points before disease symptoms emerged. The relation between transcript levels of COX and AOX ('relCOX/AOX') was found promising for plant discrimination and primer screening. Furthermore, transcript levels of xylem-harbored bacterial consortia indicated common regulation with Xf and revealed stress-induced early down-regulation and later enhancement. LPS priming promoted the earlier increase in bacterial transcripts after Xf-inoculation. This proof-of-principle study highlights a SMART perspective for AOX-assisted plant selection towards multiple-resilience that includes Xf-tolerance. It aims to support timely future plant diagnostics and in-field substitution, sustainable agro-management, which protects population diversity and strengthens both conventional breeding and high-tech, molecular breeding research. Furthermore, the results suggested early up-regulation of bacterial microbiota consortia in vascular-enriched tissues as a novel additional trait for future studies on Xf-tolerance.