Diverse Pseudomonas species engage in beneficial and suppressive interactions with the kiwifruit pathogen Psa across Actinidia germplasm

In 2010, a Pseudomonas syringae pv. actinidiae biovar 3 (Psa3) incursion into New Zealand kiwifruit orchards devastated susceptible Actinidia chinensis cultivars. In contrast, many Actinidia species maintained in germplasm collections were resistant to Psa3 and showed limited symptoms. Recent genome biosurveillance revealed the emergence of widespread leaf spot symptoms in Psa3-resistant Actinidia germplasm. Surprisingly, few Psa3 isolates were recovered from symptomatic tissues, despite the frequent isolation of phenotypical Pseudomonas isolates on selective agar. Despite the poor recovery of Psa3 isolates, Psa3 was found in all symptomatic leaf tissue through qPCR and metabarcoding analysis. Metabarcoding revealed stark differences in bacterial community composition from samples taken from lesion-carrying or lesion-free material from the same leaf. Host genotype also appeared to influence community composition but to a lesser extent. Whole genome sequencing of diverse Pseudomonas spp. isolates revealed that many belonged to the P. syringae species complex. Curiously, the kiwifruit-associated P. syringae pv. actinidifoliorum (Pfm), was never recovered, nor were any other phylogroup 1 pathovars. Pathogenicity and competitive assays revealed that while individually diverse Pseudomonas isolates were not more pathogenic than Pfm or Psa3 on resistant Actinidia hosts, they could interact with Psa to sometimes improve their growth, suggesting that these isolates may form pathogenic consortia in these disease-associated phyllosphere communities on typically Psa3-resistant hosts.