In land plants, heteroblasty broadly refers to a drastic change in morphology during growth through ontogeny. Juniperus flaccida and Pinus cembroides are conifers of independent lineages known to exhibit leaf heteroblasty between the juvenile and adult life stage of development. Juvenile leaves of P. cembroides develop spirally on the main stem and appear decurrent, flattened, and needle‐like; whereas adult photosynthetic leaves are triangular or semi‐circular needle‐like, and grow in whorls on secondary or tertiary compact dwarf shoots. By comparison, J. flaccida juvenile leaves are decurrent and needle‐like, and adult leaves are compact, short, and scale‐like. Comparative analyses were performed to evaluate differences in anatomy and gene expression patterns between developmental phases in both species. RNA from 12 samples was sequenced and analyzed with available software. They were assembled de novo from the RNA‐Seq reads. Following assembly, 63,741 high‐quality transcripts were functionally annotated in P. cembroides and 69,448 in J. flaccida. Evaluation of the orthologous groups yielded 4140 shared gene families among the four references (adult and juvenile from each species). Activities related to cell division and development were more abundant in juveniles than adults in P. cembroides, and more abundant in adults than juveniles in J. flaccida. Overall, there were 509 up‐regulated and 81 down‐regulated genes in the juvenile condition of P. cembroides and 14 up‐regulated and 22 down‐regulated genes in J. flaccida. Gene interaction network analysis showed evidence of co‐expression and co‐localization of up‐regulated genes involved in cell wall and cuticle formation, development, and phenylpropanoid pathway, in juvenile P. cembroides leaves. Whereas in J. flaccida, differential expression and gene interaction patterns were detected in genes involved in photosynthesis and chloroplast biogenesis. Although J. flaccida and P. cembroides both exhibit leaf heteroblastic development, little overlap was detected, and unique genes and pathways were highlighted in this study.
Changes in gene regulation represent an important path to generate developmental differences affecting anatomical traits. Interspecific divergence in gene expression often results from changes in transcription-stimulating enhancer elements. While gene repression is crucial for precise spatiotemporal expression patterns, the relative contribution of repressive transcriptional silencers to regulatory evolution remains to be addressed. Here, we show that the Drosophila pigmentation gene ebony has mainly evolved through changes in the spatial domains of silencers patterning its abdominal expression. By precisely editing the endogenous ebony locus of D. melanogaster, we demonstrate the requirement of two redundant abdominal enhancers and three silencers that repress the redundant enhancers in a patterned manner. We observe a role for changes in these silencers in every case of ebony evolution observed to date. Our findings suggest that negative regulation by silencers likely has an under-appreciated role in gene regulatory evolution.
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