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.

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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Genetic Variation and Evolution Study Section (GVE)
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Eckstrand, Irene A
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Donald Danforth Plant Science Center
St. Louis
United States
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Hamaji, Takashi; Kawai-Toyooka, Hiroko; Uchimura, Haruka et al. (2018) Anisogamy evolved with a reduced sex-determining region in volvocine green algae. Commun Biol 1:17
Geng, Sa; Miyagi, Ayano; Umen, James G (2018) Evolutionary divergence of the sex-determining gene MID uncoupled from the transition to anisogamy in volvocine algae. Development 145:
Coelho, Susana Margarida; Gueno, Josselin; Lipinska, Agnieszka Paulina et al. (2018) UV Chromosomes and Haploid Sexual Systems. Trends Plant Sci 23:794-807
Matt, Gavriel Y; Umen, James G (2018) Cell-Type Transcriptomes of the Multicellular Green Alga Volvox carteri Yield Insights into the Evolutionary Origins of Germ and Somatic Differentiation Programs. G3 (Bethesda) 8:531-550
Umen, James; Goodenough, Ursula; Heitman, Joseph (2017) Eukaryotic Sexual Reproduction Evoked ""with a Little Help from My Friends"". Cell 170:1059-1061
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
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
Matt, Gavriel; Umen, James (2016) Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation. Dev Biol 419:99-113
Umen, James G (2015) Lost and Found: The Secret Sex Lives of Bdelloid Rotifers. Genetics 200:409-12
Cross, Frederick R; Umen, James G (2015) The Chlamydomonas cell cycle. Plant J 82:370-92

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