Common bean resistance to Xanthomonas is associated with upregulation of the salicylic acid pathway and downregulation of photosynthesis

Abstract

Background: Common bacterial blight (CBB) caused by Xanthomonas phaseoli pv. phaseoli and Xanthomonas citri pv. fuscans is one of the major threats to common bean crops (Phaseolus vulgaris L.). Resistance to CBB is particularly complex as 26 quantitative resistance loci to CBB have been described so far. To date, transcriptomic studies after CBB infection have been very scarce and the molecular mechanisms underlying susceptibility or resistance are largely unknown. Results: We sequenced and annotated the genomes of two common bean genotypes being either resistant (BAT93) or susceptible (JaloEEP558) to CBB. Reciprocal BLAST analysis led to a list of homologs between these genotypes and the common bean reference genome (G19833), which provides a solid dataset for further comparative analyses. RNA-Seq after inoculation with X. phaseoli pv. phaseoli showed that the susceptible genotype initiated a more intense and diverse biological response than the resistant genotype. Resistance was linked to upregulation of the salicylic acid pathway and downregulation of photosynthesis and sugar metabolism, while susceptibility was linked to downregulation of resistance genes and upregulation of the jasmonic acid/ethylene pathway and of genes involved in cell wall modification.Conclusions: This study helps better understanding the mechanisms occurring during the early colonization phase of common bean by Xanthomonas and unveils new actors potentially important for resistance and susceptibility to CBB. We discuss the potential link between the pathways induced during bean colonization and genes induced by transcription activator-like effectors (TALEs), as illustrated in other Xanthomonas pathovars.

The Induction of the Isoflavone Biosynthesis Pathway Is Associated with Resistance to Common Bacterial Blight in Phaseolus vulgaris L.

“…CBB symptoms including necrotic lesions were widely apparent on X. axonopodis-inoculated leaves of the CBB-susceptible RIL, whereas symptoms were dramatically lower in the CBB-resistant RIL. The occurrence of severe symptoms in the CBB-susceptible RIL within 14 d of pathogen inoculation mirrors the disease development timeline for other P. vulgaris genotypes [4,32,33]. The accelerated development of disease symptoms in the CBB-susceptible RIL is likely because disease inoculation experiments were performed under a constant high humidity in a controlled environment.…”

“…The number of total DEGs across the 48 h PI period for both the CBB-resistant and CBB-susceptible RIL investigated in our study is well below the 2576 and 4502 DEGs respectively identified in BAT93 and JaloEEP558 leaf discs infiltrated with X. phaseoli pv. phaseoli [32]. The greater number of DEGs in the previous study could be due to the use of leaf discs for pathogen infiltration and subsequent incubation in water-agar for up to 48 h, conditions yielding approximately 200 DEGs across BAT93 and JaloEEP558 associated with nitrogen metabolism, as well as 10 photosynthesis genes.…”

“…By comparison, only one nitrogen metabolism gene with the same GO term (GO:0006807) was enriched in our study, and no photosynthesis related DEGs were enriched. The smaller complement of DEGs in our study may also be because we investigated the impact of the disease pathogen on two related RILs, rather than two unrelated P. vulgaris landraces, as was done in the previous study [32].…”

Mining endophytic microbiome information from plant and animal transcriptome data

“…In the study by Foucher et al (2020), a common bean ( Phaseolus vulgaris L.) susceptible genotype (JaloEEP558) was infected by Xanthomonas phaseoli pv. phaseoli strain CFBP6546R 48 h after inoculation (Foucher, et al, 2020). The raw RNA-Seq data of Common bean (SRA accession: SRP273448) were used.…”

Common bacterial blight of bean: a model of seed transmission and pathological convergence

“…However, expression studies related to CBB resistance are still limited (Cooper, 2015;Shi, Chaudhary, et al, 2011). Recently, a first description of whole-transcriptome changes upon infection of resistant and susceptible plants showed that resistance was associated with up-regulation of the salicylic acid pathway and downregulation of photosynthesis (Foucher et al, 2020). Interestingly, 26 genes had a large difference of expression between the resistant and susceptible genotypes and colocalized with resistance QTLs.…”