The resurrection genome of Boea hygrometrica: A blueprint for survival of dehydration

Lihong Xiao; Ge Yang; Liechi Zhang; Xinhua Yang; Shuang Zhao; Zhongzhong Ji; Qing Zhou; Min Hu; Yu Wang; Ming Chen; Yu Xu; Haijing Jin; Xuan Xiao; Guipeng Hu; Fang Bao; Yong Hu; Ping Wan; Legong Li; Xin Deng; Tingyun Kuang; Chengbin Xiang; Jian-Kang Zhu; Melvin J. Oliver; Yikun He

doi:10.1073/pnas.1505811112

New Research In

Contributed by Jian-Kang Zhu, March 26, 2015 (sent for review February 10, 2015; reviewed by Sagadevan G. Mundree and Andrew J. Wood)

Significance

The genome analysis presented here represents a major step forward in the field of desiccation tolerance and a much-anticipated resource that will have a far-reaching effect in many areas of plant biology and agriculture. We present the ∼1.69-Gb draft genome of Boea hygrometrica, an important plant model for understanding responses to dehydration. To our knowledge, this is the first genome sequence of a desiccation-tolerant extremophile, offering insight into the evolution of this important trait and a first look, to our knowledge, into the genome organization of desiccation tolerance. The underpinning genome architecture and response in relation to the hydration state of the plant and its role in the preservation of cellular integrity has important implications for developing drought tolerance improvement strategies for our crops.

Abstract

“Drying without dying” is an essential trait in land plant evolution. Unraveling how a unique group of angiosperms, the Resurrection Plants, survive desiccation of their leaves and roots has been hampered by the lack of a foundational genome perspective. Here we report the ∼1,691-Mb sequenced genome of Boea hygrometrica, an important resurrection plant model. The sequence revealed evidence for two historical genome-wide duplication events, a compliment of 49,374 protein-coding genes, 29.15% of which are unique (orphan) to Boea and 20% of which (9,888) significantly respond to desiccation at the transcript level. Expansion of early light-inducible protein (ELIP) and 5S rRNA genes highlights the importance of the protection of the photosynthetic apparatus during drying and the rapid resumption of protein synthesis in the resurrection capability of Boea. Transcriptome analysis reveals extensive alternative splicing of transcripts and a focus on cellular protection strategies. The lack of desiccation tolerance-specific genome organizational features suggests the resurrection phenotype evolved mainly by an alteration in the control of dehydration response genes.

Footnotes

↵¹To whom correspondence may be addressed. Email: jkzhu{at}purdue.edu, Mel.Oliver{at}ars.usda.gov, or yhe{at}cnu.edu.cn.

Author contributions: L.X., T.K., and Y. He designed research; L.X., G.Y., L.Z., and Z.J. performed research; Y.W., Y.X., H.J., X.X., G.H., F.B., Y. Hu, L.L., X.D., and C.X. contributed new reagents/analytic tools; L.X., X.Y., S.Z., Q.Z., M.H., M.C., P.W., J.-K.Z., M.J.O., and Y. He analyzed data; and L.X., J.-K.Z., M.J.O., and Y. He wrote the paper.
Reviewers: S.G.M., Queensland University of Technology; and A.J.W., Southern Illinois University.
The authors declare no conflict of interest.
Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE48671), and the BioSample database, www.ncbi.nlm.nih.gov/biosample (accession no. SAMN02215335).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1505811112/-/DCSupplemental.

View Full Text