Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi [Lentinus tigrinus]

The evolution of complex multicellularity has been one of the major transitions in the history of life. In contrast to simple multicellular aggregates of cells, it has evolved only in a handful of lineages, including the animals, embryophytes, red and brown algae and fungi. Despite being a key step towards the evolution of complex organisms, the evolutionary origins and the genetic underpinnings of complex multicellularity are incompletely known. We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall (FCW) remodeling, targeted protein degradation, signal transduction, adhesion and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, expansin-like proteins, protein kinases, and transcription factors, showed expansions in Agaricomycetes, with from which many convergently expandedwere identified in multicellular plants and/or animals too, assuming convergent solutions to genetic hurdles imposed by complex multicellularity among independently evolved lineages. This study provides a novel entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms. Overall design: 27 samples corresponding to 9 developmental stages were analyzed. Developmental stages contain 3 biological replicates.

复杂多细胞性的演化，乃是生命演化史上的重大转型事件之一。与简单的细胞多细胞聚集体不同，该性状仅在少数类群中独立演化而来，包括动物、有胚植物（embryophytes）、红藻、褐藻与真菌。尽管复杂多细胞性是复杂生物体演化的关键环节，但其演化起源与遗传基础仍未被完全阐明。本研究基于6个物种的发育转录组数据，以及对200余个全基因组的比较分析，构建了蘑菇子实体形成的参考图谱，旨在阐明伞菌纲（Agaricomycetes）真菌中复杂多细胞性与子实体发育的核心遗传程序。近300个保守基因家族与70余个功能类群中，均包含来自5至6个物种的发育调控基因，其功能涉及真菌细胞壁（fungal cell wall, FCW）重塑、靶向蛋白质降解、信号转导、细胞黏附以及小型分泌蛋白（包括效应蛋白样孤儿基因）等。这些家族中的多个类群，包括F-box蛋白、扩张素样蛋白、蛋白激酶与转录因子，在伞菌纲中均出现了扩张；进一步分析发现，其中许多家族在多细胞植物和/或动物中也发生了趋同演化扩张，这表明不同独立演化的类群针对复杂多细胞性带来的遗传障碍，采取了趋同的遗传解决方案。本研究为伞菌纲这一最大的复杂真核生物类群之一的蘑菇发育与复杂多细胞性研究，提供了全新的切入点。实验设计：本研究共分析了对应9个发育阶段的27个样本，每个发育阶段设置3个生物学重复。