Soil, rhizosphere, and root microbiome in kiwifruit vine decline, an emerging multifactorial disease

Micol Guaschino; Marco Garello; Luca Nari; Yeka V Zhimo; Samir Droby; Davide Spadaro

doi:10.3389/fmicb.2024.1330865

Soil, rhizosphere, and root microbiome in kiwifruit vine decline, an emerging multifactorial disease

Front Microbiol. 2024 Mar 21:15:1330865. doi: 10.3389/fmicb.2024.1330865. eCollection 2024.

Authors

Micol Guaschino^{1

2}, Marco Garello^{1

2}, Luca Nari³, Yeka V Zhimo⁴, Samir Droby⁴, Davide Spadaro^{1

2}

Affiliations

¹ Department of Agricultural, Forestry and Food Sciences (DiSAFA), University of Torino, Grugliasco, Italy.
² Interdepartmental Centre for Innovation in Agro-environmental Sector - AGROINNOVA, University of Turin, Grugliasco, Italy.
³ Fondazione Agrion, Manta, Italy.
⁴ Department of Postharvest Science, ARO, The Volcani Center, Rishon LeZion, Israel.

Abstract

Kiwifruit vine decline syndrome (KVDS) is characterized by severe root system impairment, which leads to irreversible wilting of the canopy. Plants usually collapse rapidly from the appearance of the first aboveground symptoms, without recovery even in the following seasons. The syndrome has been negatively impacting kiwifruit yield in different areas of Italy, the main producing European country, since its first outbreak in 2012. To date, a unique, common causal factor has yet to be found, and the syndrome is referred to as multifactorial. In this article, we investigated the whole biotic community (fungi, bacteria, and oomycetes) associated with the development of KVDS in three different belowground matrices/compartments (soil, rhizosphere, and root). Sampling was performed at both healthy and affected sites located in the main kiwifruit-producing area of Northwestern Italy. To address the multifactorial nature of the syndrome and to investigate the potential roles of abiotic factors in shaping these communities, a physicochemical analysis of soils was also performed. This study investigates the associations among taxonomic groups composing the microbiome and also between biotic and abiotic factors. Dysbiosis was considered as a driving event in shaping KVDS microbial communities. The results obtained from this study highlight the role of the oomycete genus Phytopythium, which resulted predominantly in the oomycete community composition of diseased matrices, though it was also present in healthy ones. Both bacterial and fungal communities resulted in a high richness of genera and were highly correlated to the sampling site and matrix, underlining the importance of multiple location sampling both geographically and spatially. The rhizosphere community associated with KVDS was driven by a dysbiotic process. In addition, analysis of the association network in the diseased rhizosphere revealed the presence of potential cross-kingdom competition for plant-derived carbon between saprobes, oomycetes, and bacteria.

Keywords: Phytopythium; dysbiosis; kiwifruit vine decline syndrome; metabarcoding; microbiome; multifactorial disease; next-generation sequencing.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was funded by Piedmont Region (Italy) with the project “KIRIS—Kiwifruit Vine Decline Syndrome: deepening the etiology and development of prevention and control tool,” by the Italian Ministry of University and Research with the project “KVD-Biome—Unveiling the plant exposome to dissect a multifactorial disease: the kiwifruit vine decline,” by AGER—Foundations Network for Agrifood Research with the project “SOS-KIWI—From SOil to Soil: origin and remediation to KIWIfruit Vine Decline Syndrome,” and by the European Commission—NextGenerationEU, Project SUS-MIRRI.IT “Strengthening the MIRRI Italian Research Infrastructure for Sustainable Bioscience and Bioeconomy,” code n. IR0000005.