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Loss of collagen gene expression in the notochord of the tailless tunicate Molgula occulta

Popsuj, Sydney; Di Gregorio, Anna; Swalla, Billie J; Stolfi, Alberto
In tunicates, several species in the Molgulidae family have convergently lost the tailed, swimming larval body plan, including the morphogenesis of the notochord, a major chordate-defining trait. Through the comparison of tailless M. occulta and a close relative, the tailed species M. oculata, we show that notochord-specific expression of the Collagen Type I/II Alpha (Col1/2a) gene appears to have been lost specifically in the tailless species. Using CRISPR/Cas9-mediated mutagenesis in the tailed laboratory model tunicate Ciona robusta, we demonstrate that Col1/2a plays a crucial role in the convergent extension of notochord cells during tail elongation. Our results suggest that the expression of Col1/2a in the notochord, although necessary for its morphogenesis in tailed species, is dispensable for tailless species. This loss is likely a result of the accumulation of cis-regulatory mutations in the absence of purifying selective pressure. More importantly, the gene itself is not lost, likely due to its roles in other developmental processes, including during the adult stage. Our study further confirms the Molgulidae as an interesting family in which to study the evolutionary loss of tissue-specific expression of otherwise indispensable genes.
PMID: 37403333
ISSN: 1557-7023
CID: 5539622

Women in tunicate research: Pioneers of the past and their present legacy

Nydam, Marie L; Saffo, Mary Beth; Di Gregorio, Anna
The search for female scientists who pioneered the research on tunicates is hindered by the tradition of reporting only the first initials of authors' names on scientific publications using only the initials of their first names. While this practice has the theoretical merit of broadening the readership by preventing the possible bias that could be caused by the gender of the author(s) in some of the readers, it rendered the identification of female researchers active in, or before, the first half of the 20th century quite challenging. Sifting through several dozen electronic records, and with the help of references and/or quotes found online, we have stitched together the information that we were able to retrieve on the life of female scientists who authored some of the earliest publications on tunicates, and we have organized them in (approximate) chronological order. We have also compiled brief synopses of the findings of scientists active in the field of tunicate biology in more recent times, and organized them by subdiscipline.
PMID: 38009445
ISSN: 1526-968x
CID: 5617882

Searching for marine embryos, finding my path [Letter]

Di Gregorio, Anna
PMID: 37994390
ISSN: 1526-968x
CID: 5608982

1st International Symposium on Women in Tunicate Biology: Meeting report [Letter]

Di Gregorio, Anna; Nydam, Marie L
PMID: 37984377
ISSN: 1526-968x
CID: 5608882

Women researchers in tunicate biology at the Stazione Zoologica Anton Dohrn in Napoli [Letter]

Di Gregorio, Anna; Locascio, Annamaria; Ristoratore, Filomena; Spagnuolo, Antonietta
PMID: 37969000
ISSN: 1526-968x
CID: 5611212

Gene expression in notochord and nuclei pulposi: a study of gene families across the chordate phylum

Raghavan, Rahul; Coppola, Ugo; Wu, Yushi; Ihewulezi, Chibuike; Negrón-Piñeiro, Lenny J; Maguire, Julie E; Hong, Justin; Cunningham, Matthew; Kim, Han Jo; Albert, Todd J; Ali, Abdullah M; Saint-Jeannet, Jean-Pierre; Ristoratore, Filomena; Dahia, Chitra L; Di Gregorio, Anna
The transition from notochord to vertebral column is a crucial milestone in chordate evolution and in prenatal development of all vertebrates. As ossification of the vertebral bodies proceeds, involutions of residual notochord cells into the intervertebral discs form the nuclei pulposi, shock-absorbing structures that confer flexibility to the spine. Numerous studies have outlined the developmental and evolutionary relationship between notochord and nuclei pulposi. However, the knowledge of the similarities and differences in the genetic repertoires of these two structures remains limited, also because comparative studies of notochord and nuclei pulposi across chordates are complicated by the gene/genome duplication events that led to extant vertebrates. Here we show the results of a pilot study aimed at bridging the information on these two structures. We have followed in different vertebrates the evolutionary trajectory of notochord genes identified in the invertebrate chordate Ciona, and we have evaluated the extent of conservation of their expression in notochord cells. Our results have uncovered evolutionarily conserved markers of both notochord development and aging/degeneration of the nuclei pulposi.
PMCID:10605842
PMID: 37891482
ISSN: 2730-7182
CID: 5610392

Xbp1 and Brachyury establish an evolutionarily conserved subcircuit of the notochord gene regulatory network

Wu, Yushi; Devotta, Arun; José-Edwards, Diana S; Kugler, Jamie E; Negrón-Piñeiro, Lenny J; Braslavskaya, Karina; Addy, Jermyn; Saint-Jeannet, Jean-Pierre; Di Gregorio, Anna
Gene regulatory networks coordinate the formation of organs and structures that compose the evolving body plans of different organisms. We are using a simple chordate model, the Ciona embryo, to investigate the essential gene regulatory network that orchestrates morphogenesis of the notochord, a structure necessary for the proper development of all chordate embryos. Although numerous transcription factors expressed in the notochord have been identified in different chordates, several of them remain to be positioned within a regulatory framework. Here, we focus on Xbp1, a transcription factor expressed during notochord formation in Ciona and other chordates. Through the identification of Xbp1-downstream notochord genes in Ciona, we found evidence of the early co-option of genes involved in the unfolded protein response to the notochord developmental program. We report the regulatory interplay between Xbp1 and Brachyury, and by extending these results to Xenopus, we show that Brachyury and Xbp1 form a cross-regulatory subcircuit of the notochord gene regulatory network that has been consolidated during chordate evolution.
PMCID:8803312
PMID: 35049502
ISSN: 2050-084x
CID: 5157112

The Degenerate Tale of Ascidian Tails

Fodor, Alexander C A; Powers, Megan M; Andrykovich, Kristin; Liu, Jiatai; Lowe, Elijah K; Brown, C Titus; Di Gregorio, Anna; Stolfi, Alberto; Swalla, Billie J
Ascidians are invertebrate chordates, with swimming chordate tadpole larvae that have distinct heads and tails. The head contains the small brain, sensory organs, including the ocellus (light) and otolith (gravity) and the presumptive endoderm, while the tail has a notochord surrounded by muscle cells and a dorsal nerve cord. One of the chordate features is a post-anal tail. Ascidian tadpoles are nonfeeding, but their tail is critical for larval locomotion. After hatching the larvae swim up towards light and are carried by the tide and ocean currents. When competent to settle, ascidian tadpole larvae swim down, away from light, to settle and metamorphose into a sessile adult. Tunicates are classified as chordates because of their chordate tadpole larvae; in contrast, the sessile adult has a U-shaped gut and very derived body plan, looking nothing like a chordate. There is one group of ascidians, the Molgulidae, where many species are known to have tailless larvae. The Swalla Lab has been studying the evolution of tailless ascidian larvae in this clade for over thirty years and has shown that tailless larvae have evolved independently several times in this clade. Comparison of the genomes of two closely related species, the tailed Molgula oculata and tailless Molgula occulta reveals much synteny, but there have been multiple insertions and deletions that have disrupted larval genes in the tailless species. Genomics and transcriptomics have previously shown that there are expressed pseudogenes in the tailless embryos, suggesting that the partial rescue of tailed features in their hybrid larvae is due to the expression of intact genes from the tailed parent. Yet surprisingly, we find that the notochord gene regulatory network is mostly intact in the tailless M. occulta, although the notochord does not converge and extend and remains as an aggregate of cells we call the "notoball". We expect that eventually many of the larval gene networks will be become evolutionarily lost in tailless ascidians and the larval body plan abandoned, with eggs developing directly into an adult. Here we review the current evolutionary and developmental evidence on how the molgulids lost their tails.
PMID: 33881514
ISSN: 1557-7023
CID: 4847162

Cis-regulatory control of stage-specific notochord gene expression by Brachyury [Meeting Abstract]

Negron-Pineiro, L. J.; Di Gregorio, A.
ISI:000651814704103
ISSN: 1540-7063
CID: 4892382

Transcription Factors of the bHLH Family Delineate Vertebrate Landmarks in the Nervous System of a Simple Chordate

Negron-Pineiro, Lenny J; Wu, Yushi; Di Gregorio, Anna
Tunicates are marine invertebrates whose tadpole-like larvae feature a highly simplified version of the chordate body plan. Similar to their distant vertebrate relatives, tunicate larvae develop a regionalized central nervous system and form distinct neural structures, which include a rostral sensory vesicle, a motor ganglion, and a caudal nerve cord. The sensory vesicle contains a photoreceptive complex and a statocyst, and based on the comparable expression patterns of evolutionarily conserved marker genes, it is believed to include proto-hypothalamic and proto-retinal territories. The evolutionarily conserved molecular fingerprints of these landmarks of the vertebrate brain consist of genes encoding for different transcription factors, and of the gene batteries that they control, and include several members of the bHLH family. Here we review the complement of bHLH genes present in the streamlined genome of the tunicate Ciona robusta and their current classification, and summarize recent studies on proneural bHLH transcription factors and their expression territories. We discuss the possible roles of bHLH genes in establishing the molecular compartmentalization of the enticing nervous system of this unassuming chordate.
PMID: 33114624
ISSN: 2073-4425
CID: 4652512