Provenances originate morphological and microbiome variation of Tuber pseudobrumale in southwestern China despite strong

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ORIGINAL ARTICLE

Provenances originate morphological and microbiome variation of Tuber pseudobrumale in southwestern China despite strong genetic consistency Dong Liu 1,2 & Mariana Herrera 1 & Fuqiang Yu 1,2 & Jesús Pèrez-Moreno 3 Received: 10 February 2020 / Revised: 26 October 2020 / Accepted: 1 November 2020 # German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Truffles are included among the most expensive fungi around the world. Around 180 truffle species have been described worldwide, and more than 50 species have been recorded from China. However, so far, the influence of provenances on truffle morphology, phylogeny, and bacterial and fungal microbiome community structure of both peridium and gleba has been scarcely studied. The rare excavated Chinese truffle Tuber pseudobrumale, known previously only from its type collection, was investigated in different collections from Yunnan and Sichuan provinces located in southwestern China. The microbiome showed differences at the phylum and order levels according to their provenances and compartments (gleba or peridium). For the first time, yeasts and filamentous fungi associated with truffles were studied using a metagenomic approach. Sixty-one fungal genera were identified by Illumina high throughput sequencing, belonging to 48 families, 37 orders, 20 classes, and 11 phyla were recorded. The non-metric multi-dimensional scaling plots (NDMS) showed different patterns for bacteria and fungi. In bacteria, both compartments and provenances were grouped in different clusters, while fungi grouped together more by provenance than by compartments. These changes were recorded along with macro- and micromorphological variations of the ascomata in the different collections. This integral study demonstrates for the first time that the provenances originate conspicuous intraspecific variations in T. pseudobrumale in terms of morphology and microbiome community structure in peridium and gleba, despite strong genetic consistency. Keywords Microbiome . Truffle compartments . Intraspecific variations . Fungal diversity . Geographic locations

Introduction In the northern hemisphere, the genus Tuber is one of the most diverse groups of ascomycete hypogeous fungi that form Section Editor: Martin Rühl * Fuqiang Yu [email protected] * Jesús Pèrez-Moreno [email protected]; [email protected] 1

Germplasm Bank of Wild Species in Southwestern China, Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China

2

SWFU-KIB CAS Joint Institute for Applied Mycology, Kunming, Yunnan, China

3

Colegio de Postgraduados, Campus Montecillo, Microbiología, Edafología, Texcoco, Mexico

fruiting bodies called truffles (Bonito et al. 2010; Vahdatzadeh et al. 2015). It includes some of the most expensive species of edible fungi whose international commerce worth is hundreds of millions of American dollars annually, in particular T. magnatum and T. melanosporum (Mello et al.