Deeply Altered Genome Architecture in the Endoparasitic Flowering Plant Sapria himalayana Griff. (Rafflesiaceae)

Cai L 1 , Arnold BJ 2 , Xi Z 3 , Khost DE 2 , Patel N 4 , Hartmann CB 5 Show all authors , Manickam S 6 , Sasirat S 7 , Nikolov LA 8 , Mathews S 9 , Sackton TB 10 , Davis CC 11

Affiliations 

  • 1 Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA; Harvard University Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA
  • 2 FAS Informatics Group, Harvard University, 38 Oxford Street, Cambridge, MA 02138, USA
  • 3 Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China
  • 4 Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Road, Unit 3043, Storrs, CT 06269, USA
  • 5 Bauer Core Facilities, Division of Science, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA
  • 6 Rimba Ilmu Botanic Garden, Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia
  • 7 Queen Sirikit Botanic Garden, PO Box 7 Mae Rim, Chiang Mai 50180, Thailand
  • 8 Department of Molecular, Cell and Developmental Biology, and Molecular Biology Institute, University of California, Los Angeles, 610 Charles E Young Drive East, Los Angeles, CA 90095, USA
  • 9 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70808, USA
  • 10 FAS Informatics Group, Harvard University, 38 Oxford Street, Cambridge, MA 02138, USA. Electronic address: tsackton@g.harvard.edu
  • 11 Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA; Harvard University Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA. Electronic address: cdavis@oeb.harvard.edu
Curr Biol, 2021 03 08;31(5):1002-1011.e9.
PMID: 33485466 DOI: 10.1016/j.cub.2020.12.045

Abstract

Despite more than 2,000-fold variation in genome size, key features of genome architecture are largely conserved across angiosperms. Parasitic plants have elucidated the many ways in which genomes can be modified, yet we still lack comprehensive genome data for species that represent the most extreme form of parasitism. Here, we present the highly modified genome of the iconic endophytic parasite Sapria himalayana Griff. (Rafflesiaceae), which lacks a typical plant body. First, 44% of the genes conserved in eurosids are lost in Sapria, dwarfing previously reported levels of gene loss in vascular plants. These losses demonstrate remarkable functional convergence with other parasitic plants, suggesting a common genetic roadmap underlying the evolution of plant parasitism. Second, we identified extreme disparity in intron size among retained genes. This includes a category of genes with introns longer than any so far observed in angiosperms, nearing 100 kb in some cases, and a second category of genes with exceptionally short or absent introns. Finally, at least 1.2% of the Sapria genome, including both genic and intergenic content, is inferred to be derived from host-to-parasite horizontal gene transfers (HGTs) and includes genes potentially adaptive for parasitism. Focused phylogenomic reconstruction of HGTs reveals a hidden history of former host-parasite associations involving close relatives of Sapria's modern hosts in the grapevine family. Our findings offer a unique perspective into how deeply angiosperm genomes can be altered to fit an extreme form of plant parasitism and demonstrate the value of HGTs as DNA fossils to investigate extinct symbioses.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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