Gene-rich UV sex chromosomes harbor conserved regulators of sexual development

Carey, Sarah B.; Jenkins, Jerry; Lovell, John T; Maumus, Florian; Sreedasyam, Avinash; Payton, Adam C.; Shu, Shengqiang; Tiley, George P.; Fernandez-Pozo, Noé; Healey, Adam; Barry, Kerrie; Chen, Cindy; Wang, Mei; Lipzen, Anna; Daum, Chris; Saski, Christopher; McBreen, Jordan C.; Conrad, Roth E.; Kollar, Leslie M.; Olsson, Sanna; Huttunen, Sanna; Landis, Jacob B.; Burleigh, J. Gordon; Wickett, Norman J.; Johnson, Matthew G.; Rensing, Stefan A.; Grimwood, Jane; Schmutz, Jeremy; McDaniel, Stuart F.

doi:10.1126/sciadv.abh2488

Cited by 73 publications

(84 citation statements)

References 122 publications

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“…However, no sMYB - PRR linkage was detected in these genomes at either short or long distance; many of these genome assemblies are not chromosome-resolved, which could mean the linkage would be missed if it were on the scale found in Amborella . In addition, two chromosome-resolved moss genomes of Physcomitrium patens (formerly Physcomatrella patens ) and Ceratodon purpureus have the sMYB and PRR on separate chromosomes and therefore clearly unlinked (Lang et al, 2018; Carey et al, 2021). A chromosome-resolved genome assembly of a bryophyte is available for Sphagnum angustifolium (formally Sphagnum fallax ), which provides an opportunity to evaluate a third moss genome (Meleshko et al, 2021).…”

Section: Resultsmentioning

confidence: 99%

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Michael

2021

Preprint

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The circadian clock ensures that biological processes are phased to the correct time of day. In plants the circadian clock is conserved at both the level of transcriptional networks as well as core genes. In the model plant Arabidopsis thaliana, the core circadian singleMYB (sMYB) genes CCA1 and RVE4 are in genetic linkage with the PSEUDO-RESPONSE REGULATOR (PRR) genes PRR9 and PRR7 respectively. Leveraging chromosome-resolved plant genomes and syntenic ortholog analysis it was possible to trace this genetic linkage back to the basal angiosperm Amborella and identify an additional evolutionarily conserved genetic linkage between PIF3 and PHYA. The LHY/CCA1-PRR5/9, RVE4/8-PRR3/7 and PIF3-PHYA genetic linkages emerged in the bryophyte lineage and progressively moved within several genes of each other across an array of higher plant families representing distinct whole genome duplication and fractionation events. Soybean maintains all but two genetic linkages, and expression analysis revealed the PIF3-PHYA linkage overlapping with the E4 maturity group locus was the only pair to robustly cycle with an evening phase in contrast to the sMYB-PRR morning and midday phase. While most monocots maintain the genetic linkages, they have been lost in the economically important grasses (Poaceae) such as maize where the genes have been fractionated to separate chromosomes and presence/absence variation results in the segregation of PRR7 paralogs across heterotic groups. The evolutionary conservation of the genetic linkage as well as its loss in the grasses provides new insight in the plant circadian clock, which has been a critical target of breeding and domestication.Summary SentenceThe genetic linkage of the core circadian clock components has evolutionary origins in bryophytes and sheds light on the current functioning and selection on the circadian clock in crops.

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Section: Resultsmentioning

confidence: 99%

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Michael

2021

Preprint

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“… 18 Further, haploid plants spontaneously containing both U and V chromosomes develop as females, supporting the presence of a dominant U-linked feminizing locus, 22 in whose absence plants develop as males. Genomic analyses of M. polymorpha have shown that both U and V chromosomes have lower gene densities, and higher repetitive content, than the autosomes, 19 , 20 , 21 similar to the symmetrical changes in other non-recombining U/V systems, in the mosses Ceratodon purpureus 23 and Syntrichia caninervis 24 and the brown alga Ectocarpus . 25 However, the sex-determining genes have yet to be identified in liverworts or any other complex multicellular haploid organism, and only recently has it become possible to study the evolution of sex chromosomes in haploid systems and test their predicted differences from diploid systems.…”

Section: Introductionmentioning

confidence: 82%

Identification of the sex-determining factor in the liverwort Marchantia polymorpha reveals unique evolution of sex chromosomes in a haploid system

et al. 2021

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Summary Sex determination is a central process for sexual reproduction and is often regulated by a sex determinant encoded on a sex chromosome. Rules that govern the evolution of sex chromosomes via specialization and degeneration following the evolution of a sex determinant have been well studied in diploid organisms. However, distinct predictions apply to sex chromosomes in organisms where sex is determined in the haploid phase of the life cycle: both sex chromosomes, female U and male V, are expected to maintain their gene functions, even though both are non-recombining. This is in contrast to the X-Y (or Z-W) asymmetry and Y (W) chromosome degeneration in XY (ZW) systems of diploids. Here, we provide evidence that sex chromosomes diverged early during the evolution of haploid liverworts and identify the sex determinant on the Marchantia polymorpha U chromosome. This gene, Feminizer , encodes a member of the plant-specific BASIC PENTACYSTEINE transcription factor family. It triggers female differentiation via regulation of the autosomal sex-determining locus of FEMALE GAMETOPHYTE MYB and SUPPRESSOR OF FEMINIZATION . Phylogenetic analyses of Feminizer and other sex chromosome genes indicate dimorphic sex chromosomes had already been established 430 mya in the ancestral liverwort. Feminizer also plays a role in reproductive induction that is shared with its gametolog on the V chromosome, suggesting an ancestral function, distinct from sex determination, was retained by the gametologs. This implies ancestral functions can be preserved after the acquisition of a sex determination mechanism during the evolution of a dominant haploid sex chromosome system.

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“…Although, plant sex chromosomes are not without consequences from suppressed recombination. A consistent pattern found is an enrichment of transposable elements (TEs) and other repeats [65,[76][77][78], which often accumulate in regions of low recombination [79]. In fact, in several species TE expansions have instead driven the Y chromosome to be larger than the X, such as in Coccinia grandis [80] and S. latifolia [81].…”

Section: "The Discovery Referred To In a Preceding Footnote That The Spermatogonial Number Of Anasa Is 21 Instead Of 22 Again Goes Far Tomentioning

confidence: 93%

“…However, some plant sex chromosomes defy these expectations. The moss UV sex chromosomes evolved hundreds of millions of years ago but are homomorphic in Ceratodon purpureus [65]. Similarly, in Cannabis sativa the sex chromosomes share an origin with H. lupulus [62], however, they are instead homomorphic.…”

Section: "The Discovery Referred To In a Preceding Footnote That The Spermatogonial Number Of Anasa Is 21 Instead Of 22 Again Goes Far Tomentioning

confidence: 99%

“…Estimates of divergence between XY genes in R. hastatulus sex suggest a minimum age of 9 million years [71], and while some genes have also been lost on the Y [72], pollenexpressed genes are significantly less likely to be lost than those expressed in diploid tissues [71,73]. The haploid C. purpureus UV sex chromosomes contain over 3,400 genes each, half of which were shown to be expressed in the gametophytes [65]. The lack of degeneration could also be due to the small size of the SDR seen in many plants.…”

Section: "The Discovery Referred To In a Preceding Footnote That The Spermatogonial Number Of Anasa Is 21 Instead Of 22 Again Goes Far Tomentioning

confidence: 99%

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The contributions of Dr. Nettie Stevens to the field of sex chromosome biology

Carey¹,

Aközbek²,

Harkess³

2021

Preprint

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The early 1900s delivered many foundational discoveries in genetics, including re-discovery of Mendel’s research and the chromosomal theory of inheritance. Following these insights, many focused their research on whether the development of separate sexes had a chromosomal basis or if instead it was caused by environmental factors. It is Dr. Nettie M. Stevens’ Studies in Spermatogenesis (1905) that provided the unequivocal evidence that the inheritance of the Y chromosome initiated male development in mealworms. This result established that sex is indeed a Mendelian trait with a genetic basis, and that the sex chromosomes play a critical role. In part II of Studies in Spermatogenesis (1906) an XY pair was identified in dozens of additional species, further validating the function of sex chromosomes. Since this formative work, a wealth of studies in animals and plants have examined the genetic basis of sex. The goal of this review is to shine a light again on Stevens’ Studies in Spermatogenesis and the lasting impact of this work. We additionally focus on key findings in plant systems over the last century and open questions that are best answered, as in Stevens’ work, by synthesizing across many systems.

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Gene-rich UV sex chromosomes harbor conserved regulators of sexual development

Cited by 73 publications

References 122 publications

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Identification of the sex-determining factor in the liverwort Marchantia polymorpha reveals unique evolution of sex chromosomes in a haploid system

The contributions of Dr. Nettie Stevens to the field of sex chromosome biology

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