The long-term goal of our work is to understand the role of sex chromosomes in the evolution of complex developmental traits. Dimorphic sexes (eggs and sperm) are a fundamental strategy for reproductive success in multicellular organisms, yet almost nothing is known about how two different sexes evolved from a proposed unicellular ancestor with morphologically identical mating types. Volvox carteri is a multicellular green alga that is sexually dimorphic and is closely related to Chlamydomonas reinhardtii, a non-dimorphic unicell. In both algal species sexual differentiation is controlled by a multigenic haploid mating locus (MT). MT in Volvox has undergone a remarkable expansion relative to MT from Chlamydomonas and acquired the properties of a sex chromosome. Our data suggest that rapid evolution of Volvox MT genes through largely non-adaptive processes provided raw material for sexual selection and genetic innovation. We propose to test four sources of such innovation that arose in Volvox MT and how they contributed to the evolution of dimorphic sexes: 1. Remodeling of gene regulatory network inputs for a male sex determination gene, vcMid. We will test whether vcMid protein is regulated post-transcriptionally in response to sex inducer or is regulated post- translationally. We will inactivate vcMid using RNAi to determine whether its absence is sufficient to induce oogenesis. We will use trans-species complementation to determine the key changes that allowed vcMid to become a spermatogenesis factor in Volvox. 2. Remodeling of gene regulatory network outputs for vcMid. Female Volvox that express a vcMid transgene (Eve::Mid-T) produce sperm. We will use quantitative RNA-seq data from females, males, Eve::Mid-T lines, and vcMid knockdown lines to identify the vcMid-regulated target genes that control spermatogenesis and female MT genes that control oogenesis. 3. The cooption and divergence of a shared MT gene, MAT3. We will determine whether the female and male alleles, MAT3-f and MAT3-m, control early embryonic germ cell cycle patterning by reciprocal knockdowns and replacements. The mechanism of sex-regulated alternative MAT3 splicing will be investigated. 4. Formation of new genes. HMG1 and FSI1 are new female MT genes with no known homologs. Epitope tagging, RNAi knockdowns and mis-expression will be used to test their predicted contributions to female egg identity and gamete recognition, respectively. Conservation of other novel male and female MT genes will be investigated in related species. Our findings on how dimorphism evolved in volvocine algae are likely to have general significance for understanding the origin of sex chromosomes and their contribution to large-scale evolutionary changes. In addition, many human genetic diseases are linked to sex chromosomes or are impacted by gender, and this work will help elucidate the general principles that govern the etiology of such diseases. !

Public Health Relevance

Many human diseases are linked to sex chromosomes or have etiologies that are significantly affected by gender. This proposal investigates the origins of gender and sex chromosomes in a model organism, Volvox carteri, whose development and evolution has many parallels with humans and other animals. The knowledge obtained from our studies will provide fundamental information on sex chromosome biology that may lead to a better understanding of human sex-linked diseases.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM078376-08
Application #
8539632
Study Section
Genetic Variation and Evolution Study Section (GVE)
Program Officer
Eckstrand, Irene A
Project Start
2006-06-27
Project End
2015-06-30
Budget Start
2013-07-01
Budget End
2014-06-30
Support Year
8
Fiscal Year
2013
Total Cost
$318,450
Indirect Cost
$125,450
Name
Donald Danforth Plant Science Center
Department
Type
DUNS #
044193006
City
St. Louis
State
MO
Country
United States
Zip Code
63132
Matt, Gavriel; Umen, James (2016) Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation. Dev Biol 419:99-113
Hamaji, Takashi; Mogi, Yuko; Ferris, Patrick J et al. (2016) Sequence of the Gonium pectorale Mating Locus Reveals a Complex and Dynamic History of Changes in Volvocine Algal Mating Haplotypes. G3 (Bethesda) 6:1179-89
Hamaji, Takashi; Lopez, David; Pellegrini, Matteo et al. (2016) Identification and Characterization of a cis-Regulatory Element for Zygotic Gene Expression in Chlamydomonas reinhardtii. G3 (Bethesda) 6:1541-8
Cross, Frederick R; Umen, James G (2015) The Chlamydomonas cell cycle. Plant J 82:370-92
Umen, James G (2015) Lost and Found: The Secret Sex Lives of Bdelloid Rotifers. Genetics 200:409-12
Lopez, David; Hamaji, Takashi; Kropat, Janette et al. (2015) Dynamic Changes in the Transcriptome and Methylome of Chlamydomonas reinhardtii throughout Its Life Cycle. Plant Physiol 169:2730-43
Geng, Sa; De Hoff, Peter; Umen, James G (2014) Evolution of sexes from an ancestral mating-type specification pathway. PLoS Biol 12:e1001904
Fang, Su-Chiung; Chung, Chin-Lin; Chen, Chun-Han et al. (2014) Defects in a new class of sulfate/anion transporter link sulfur acclimation responses to intracellular glutathione levels and cell cycle control. Plant Physiol 166:1852-68
Umen, James G (2014) Green algae and the origins of multicellularity in the plant kingdom. Cold Spring Harb Perspect Biol 6:a016170
Umen, James; Heitman, Joseph (2013) Evolution of sex: mating rituals of a pre-metazoan. Curr Biol 23:R1006-8

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