Innovation and constraint leading to complex multicellularity in the Ascomycota.
The advent of complex multicellularity (CM) was a pivotal event in the evolution of animals, plants and fungi. In the fungal Ascomycota, CM is based on hyphal filaments and arose in the Pezizomycotina. The genus Neolecta defines an enigma: phylogenetically placed in a related group containing mostly yeasts, Neolecta nevertheless possesses Pezizomycotina-like CM. Here we sequence the Neolecta irregularis genome and identify CM-associated functions by searching for genes conserved in Neolecta and the Pezizomycotina, which are absent or divergent in budding or fission yeasts. This group of 1,050 genes is enriched for functions related to diverse endomembrane systems and their organization. Remarkably, most show evidence for divergence in both yeasts. Using functional genomics, we identify new genes involved in fungal complexification. Together, these data show that rudimentary multicellularity is deeply rooted in the Ascomycota. Extensive parallel gene divergence during simplification and constraint leading to CM suggest a deterministic process where shared modes of cellular organization select for similarly configured organelle- and transport-related machineries.
Temasek Life Sciences Laboratory and Department of Biological Sciences, The National University of Singapore, Singapore 117604, Singapore.
Tu Anh
TA
Nguyen
Department of Plant Pathology and Microbiology, Institute for Integrative Genome Biology, University of California-Riverside, Riverside, California 92521, USA.
Ousmane H
OH
Cissé
Temasek Life Sciences Laboratory and Department of Biological Sciences, The National University of Singapore, Singapore 117604, Singapore.
Jie
J
Yun Wong
Temasek Life Sciences Laboratory and Department of Biological Sciences, The National University of Singapore, Singapore 117604, Singapore.
Peng
P
Zheng
Department of Botany, Academy of Natural Sciences of Philadelphia, Philadelphia, Pennsylvania 19103, USA.
David
D
Hewitt
Lehrstuhl für Allgemeine und Molekulare Botanik, Ruhr-Universität Bochum, 44780 Bochum, Germany.
Minou
0000-0003-0075-6695
M
Nowrousian
Department of Plant Pathology and Microbiology, Institute for Integrative Genome Biology, University of California-Riverside, Riverside, California 92521, USA.
Jason E
0000-0002-7591-0020
JE
Stajich
Temasek Life Sciences Laboratory and Department of Biological Sciences, The National University of Singapore, Singapore 117604, Singapore.
Gregory
G
Jedd
D001203:Ascomycota / Q000166:cytology* / Q000235:genetics; D044822:Biodiversity; D001692:Biological Transport / Q000502:physiology; D019295:Computational Biology; D004271:DNA, Fungal / Q000235:genetics*; D019143:Evolution, Molecular; D005656:Fungal Proteins / Q000502:physiology*; D016681:Genome, Fungal / Q000502:physiology*; D010802:Phylogeny; D016415:Sequence Alignment; D000073336:Whole Genome Sequencing
D004271:DNA, Fungal; D005656:Fungal Proteins