TY - JOUR
T1 - A bird-like genome from a frog
T2 - Mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum
AU - Lamichhaney, Sangeet
AU - Catullo, Renee
AU - Keogh, J. Scott
AU - Clulow, Simon
AU - Edwards, Scott V.
AU - Ezaz, Tariq
N1 - Funding Information:
We thank Simon Yung Wa Sin and Daren Card (Harvard University) for laboratory assistance in preparing sequencing libraries of P. ornatum; Zuzana Majtanova, Foyez Shams, and Rod Ubrihien for laboratory assistance in tissue collections, chromosome preparation, and karyotyping; Jodi Rowley for providing samples of Li. fletcheri and Le. Fletcheri; and the curators and curatorial associates of the Department of Herpetology of the Museum of Comparative Zoology at Harvard University for assistance with sample transportation and storage. We thank Yong Zhang for helpful comments on early drafts of this manuscript, the three reviewers for helpful reviews, and Jim Hanken for helpful discussion in the early stages of this project. We thank Christoph Liedtke and Ivan Gomez-Mestre for their help in placing Platyplectrum genome size change in context. Additional sequencing was performed at the Harvard University Bauer Core Facility and we thank the staff for assistance. Computations were performed on the Cannon computing cluster at Harvard University and supported by Harvard Research Computing. This work was supported in part by an internal research grant by the Institute for Applied Ecology, University of Canberra (to T.E.). S.L. was supported by a Wenner Gren Postdoctoral Fellowship. J.S.K. thanks the Australian Research Council for ongoing support. S.V.E. thanks the National Science Foundation and Harvard University for support. Page charges for this paper were covered in part by a grant from the Wetmore Colles Fund of the Museum of Comparative Zoology.
Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.
Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2021/3/16
Y1 - 2021/3/16
N2 - The diversity of genome sizes across the tree of life is of key interest in evolutionary biology. Various correlates of variation in genome size, such as accumulation of transposable elements (TEs) or rate of DNA gain and loss, are well known, but the underlying molecular mechanisms driving or constraining genome size are poorly understood. Here, we study one of the smallest genomes among frogs characterized thus far, that of the ornate burrowing frog (Platyplectrum ornatum) from Australia, and compare it to other published frog and vertebrate genomes to examine the forces driving reduction in genome size. At ∼1.06 gigabases (Gb), the P. ornatum genome is like that of birds, revealing four major mechanisms underlying TE dynamics: reduced abundance of all major classes of TEs; increased net deletion bias in TEs; drastic reduction in intron lengths; and expansion via gene duplication of the repertoire of TE-suppressing Piwi genes, accompanied by increased expression of Piwi-interacting RNA (piRNA)-based TEsilencing pathway genes in germline cells. Transcriptomes from multiple tissues in both sexes corroborate these results and provide insight into sex-differentiation pathways in Platyplectrum. Genome skimming of two closely related frog species (Lechriodus fletcheri and Limnodynastes fletcheri) confirms a reduction in TEs as a major driver of genome reduction in Platyplectrum and supports a macroevolutionary scenario of small genome size in frogs driven by convergence in life history, especially rapid tadpole development and tadpole diet. The P. ornatum genome offers a model for future comparative studies on mechanisms of genome size reduction in amphibians and vertebrates generally.
AB - The diversity of genome sizes across the tree of life is of key interest in evolutionary biology. Various correlates of variation in genome size, such as accumulation of transposable elements (TEs) or rate of DNA gain and loss, are well known, but the underlying molecular mechanisms driving or constraining genome size are poorly understood. Here, we study one of the smallest genomes among frogs characterized thus far, that of the ornate burrowing frog (Platyplectrum ornatum) from Australia, and compare it to other published frog and vertebrate genomes to examine the forces driving reduction in genome size. At ∼1.06 gigabases (Gb), the P. ornatum genome is like that of birds, revealing four major mechanisms underlying TE dynamics: reduced abundance of all major classes of TEs; increased net deletion bias in TEs; drastic reduction in intron lengths; and expansion via gene duplication of the repertoire of TE-suppressing Piwi genes, accompanied by increased expression of Piwi-interacting RNA (piRNA)-based TEsilencing pathway genes in germline cells. Transcriptomes from multiple tissues in both sexes corroborate these results and provide insight into sex-differentiation pathways in Platyplectrum. Genome skimming of two closely related frog species (Lechriodus fletcheri and Limnodynastes fletcheri) confirms a reduction in TEs as a major driver of genome reduction in Platyplectrum and supports a macroevolutionary scenario of small genome size in frogs driven by convergence in life history, especially rapid tadpole development and tadpole diet. The P. ornatum genome offers a model for future comparative studies on mechanisms of genome size reduction in amphibians and vertebrates generally.
KW - Anura
KW - Frog
KW - Intron
KW - Piwi genes
KW - Transposable elements
UR - http://www.scopus.com/inward/record.url?scp=85102374284&partnerID=8YFLogxK
U2 - 10.1073/pnas.2011649118
DO - 10.1073/pnas.2011649118
M3 - Article
C2 - 33836564
AN - SCOPUS:85102374284
SN - 0027-8424
VL - 118
SP - 1
EP - 12
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 11
M1 - e2011649118
ER -