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Comparing dormancy in two distantly related tunicates reveals morphological, molecular, and ecological convergences and repeated co-option

ABSTRACT: Many asexually-propagating marine invertebrates can survive extreme environmental conditions by developing dormant structures, i.e., morphologically simplified bodies that retain the capacity to completely regenerate a functional adult when conditions return to normal. Here, we examine the environmental, morphological, and molecular characteristics of dormancy in two distantly related clonal tunicate species: Polyandrocarpa zorritensis and Clavelina lepadiformis. In both species, we report that the dormant structures are able to withstand harsher temperature and salinity conditions compared to the adult, and are the dominant forms these species employ to survive the colder winter months. By finely controlling the entry and exit of dormancy in laboratory-reared individuals, we were able to select and characterize the morphology of dormant structures associated with their transcriptome dynamics. In both species, we identified putative stem and nutritive cells in structures that resemble the earliest stages of asexual propagation. By characterizing gene expression during dormancy and regeneration into the adult body plan (i.e., germination), we observed that genes which control dormancy and environmental sensing in other metazoans, notably HIF-α and insulin signaling genes, are also expressed in tunicate dormancy. Germination-related genes in these two species, such as the retinoic acid pathway, are also found in other unrelated clonal tunicates during asexual development. These results are suggestive of repeated exaptation of conserved eco-physiological and regeneration programs for the origin of novel dormancy-germination processes across distantly related animal taxa.

ORGANISM(S): Clavelina lepadiformis Polyandrocarpa zorritensis

PROVIDER: GSE198056 | GEO | 2022/07/27

REPOSITORIES: GEO

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Project description:Plant embryos can survive years in a desiccated, quiescent state within seeds. In many species, seeds are dormant and unable to germinate at maturity. They acquire the capacity to germinate through a period of dry storage called after-ripening (AR), a biological process that occurs at 5-15% moisture when most metabolic processes cease. Because stored transcripts will be among the first proteins translated upon water uptake, they likely impact germination potential. Transcriptome changes associated with the increased seed dormancy of the GA-insensitive sly1-2 mutant, and with dormancy loss through sly1-2 after-ripening or constitutive overexpression of the GA receptor (GID1b) were characterized in dry seeds. This experiment used the same seed batches as a previous experiment (E-MTAB-4782) to characterize transcriptional changes associated with the increased seed dormancy and dormancy loss in imbibing seeds. The SLY1 gene encodes the F-box subunit of an SCF E3 ubiquitin ligase needed for GA-triggered proteolysis of DELLA repressors of seed germination. In the sly1-2 mutant, GA-directed DELLA proteolysis cannot occur leading to DELLA protein accumulation and increased dormancy. sly1-2 mutant seeds are fully dormant at 2 weeks of dry storage (0% germination), but germinate well with very long after-ripening (51% germination after 19 months). sly1-2 seed germination can also be rescued by overexpression of the GA receptor, GA-INSENSITIVE DWARF1b (GID1b-OE), which resulted in 74% germination at 2 weeks of dry storage. In this experiment, we sampled dry seeds of wild-type Ler at 2 weeks of dry storage (non-dormant), dormant sly1-2 (2 weeks of dry storage; sly1-2(D)), long after-ripened sly1-2 (non-dormant, 19 months of dry storage; sly1-2(AR)), and sly1-2 GID1b-OE (non-dormant, 2 weeks of dry storage). This experimental design allowed comparison between these transcriptomes in dry seeds to determine if dry seed stored mRNA differences contribute to the dormancy phenotypes observed once seeds are imbibed. Seeds for Ler wt, sly1-2(D), and sly1-2 GID1b-OE were grown alongside each other under the same conditions and after-ripened for 2 weeks. Seeds from sly1-2(AR) were grown under the same conditions in advance of the other lines to allow for the long after-ripening requirement. RNA was extracted using a phenol-chloroform-based extraction from three biological replicates per treatment.

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Comparing dormancy in two distantly related tunicates reveals morphological, molecular, and ecological convergences and repeated co-option

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