University of Illinois Urbana-Champaign

Dissecting the evolutionary forces shaping sex chromosome evolution in papaya

Vanburen, Robert

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https://hdl.handle.net/2142/49675

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Title
Dissecting the evolutionary forces shaping sex chromosome evolution in papaya
Author(s)
Vanburen, Robert
Issue Date
2014-05-30T17:04:12Z
Director of Research (if dissertation) or Advisor (if thesis)
Ming, Ray R.
Doctoral Committee Chair(s)
Ming, Ray R.
Committee Member(s)
  • Jacobs, Thomas W.
  • Caetano-Anollés, Gustavo
  • Hanzawa, Yoshie
Department of Study
Plant Biology
Discipline
Plant Biology
Degree Granting Institution
University of Illinois at Urbana-Champaign
Degree Name
Ph.D.
Degree Level
Dissertation
Date of Ingest
2014-05-30T17:04:12Z
Keyword(s)
  • sex chromosomes
  • evolution
  • degeneration
  • suppressed recombination
Abstract
The human Y chromosome is an ancient relic of its autosomal precursor; most of the genes have been lost in its 166 million years of separation from the X, and it has drastically shrunken in size. The highly degenerated nature of the human sex chromosomes make it impossible to trace the events that lead to their inception. Several theories have been proposed for how sex chromosomes evolve and the forces that shape their evolution, but complete sequence information is needed to test these hypotheses. Sex chromosomes in mammals are ancient, but sex chromosomes in fish, birds, and plants are much younger. The sex chromosomes of papaya evolved around 7 million years ago, making them an excellent model for studying the early stages of sex chromosome evolution. The papaya sex chromosomes are differentiated by an 8.1 Mbp, recombinationally suppressed, hermaphrodite-specific or male-specific region on the Y chromosome (HSY or MSY respectively) and its 3.5 Mb X counterpart. The X and HSY have been sequenced completely, shedding light on the early events of sex chromosome evolution. From their inception, Y chromosomes in plants and animals are subjected to the powerful effects of Müller’s ratchet, a process spurred by suppression of recombination that results in a rapid accumulation of mutations and repetitive elements. The HSY has ballooned to 2.5 times the size of the X, accumulating a staggering amount of repeat sequences. The papaya Y, in the absence of recombination has accumulated nearly 12 times the amount of chloroplast-derived DNA than the corresponding region of the X chromosome and 4 times the papaya genome-wide average. Furthermore, a chloroplast genome fragment containing the rsp15 gene has been amplified 23 times in the HSY, evidence of retrotransposon-mediated duplication. The accumulated chloroplast DNA is evidence of the slow degeneration of the HSY. To characterize the forces shaping Y chromosome evolution, we sequenced the MSY using a BAC by BAC approach and used whole genome resequencing on 12 cultivated hermaphordites and 24 wild males. The MSY and hermaphrodite specific region of the Yh (HSY) are highly similar with shared gene content and structure. The Y chromosomes form three distinct populations despite otherwise normal gene flow in the autosomes. Molecular dating suggests the hermaphrodite Y chromosome is a product of human domestication about 4,000 years ago in Mesoamerica from a wild dioecious population now distributed into the north pacific region of Costa Rica. The papaya Y chromosomes have a higher diversity than the autosome, contrasting other young chromosome systems. The autosomal regions and male Y chromosome are evolving neutrally, but the HSY is experiencing strong positive selection due to a selective sweep during human domestication. This is the first case where human domestication resulted in the evolution of a new Y chromosome with novel functions which subject it to unique evolutionary constraints. The whole genome resequencing data was also used to assess the diversity, population structure, and selective forces acting on the X chromosome in papaya. Despite separate breeding systems of dioecy and gynodioecy, the X chromosomes are highly similar and cluster into a single group. This contrasts the two sub groups (gynodioecy and dioecy) observed in the autosome and three sub groups observed in the Y. The X chromosome has a tenfold reduction in nucleotide diversity compared to the autosome. This reduced diversity is caused by large scale selective sweeps and genetic bottleneck on the X. The low nucleotide diversity and strong selective sweep distinguish papaya from other sex chromosome systems. Together these results drastically expand our current knowledge if the evolutionary processes and forces that shape young sex chromosome evolution.
Graduation Semester
2014-05
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Copyright 2014 Robert Vanburen

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