Next generation limb development and evolution: old questions, new perspectives

Zúñiga, Aimée

doi:10.1242/dev.125757

Cited by 126 publications

(116 citation statements)

References 120 publications

(162 reference statements)

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“…Notably, our model has implications for the existence of inverse hourglasses in additional development contexts, such as leaves (Freeling 1992;Ori et al 2007;Ichihashi et al 2014;Alvarez et al 2016). This further raises the exciting possibility that transcriptome inverse hourglasses exist in other developmental programs beyond plants, such as in animal lung and limb development, in which tissue ontogeny is associated with organ complexity (Metzger et al 2008;Zuniga 2015).…”

Section: Wwwgenomeorgmentioning

confidence: 88%

The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation

et al. 2016

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One of the most remarkable manifestations of plant evolution is the diversity for floral branching systems. These "inflorescences" arise from stem cell populations in shoot meristems that mature gradually to reproductive states in response to environmental and endogenous signals. The morphology of the shoot meristem maturation process is conserved across distantly related plants, raising the question of how diverse inflorescence architectures arise from seemingly common maturation programs. In tomato and related nightshades (Solanaceae), inflorescences range from solitary flowers to highly branched structures bearing hundreds of flowers. Since reproductive barriers between even closely related Solanaceae have precluded a genetic dissection, we captured and compared meristem maturation transcriptomes from five domesticated and wild species reflecting the evolutionary continuum of inflorescence complexity. We find these divergent species share hundreds of dynamically expressed genes, enriched for transcription factors. Meristem stages are defined by distinct molecular states and point to modified maturation schedules underlying architectural variation. These modified schedules are marked by a peak of transcriptome expression divergence during the reproductive transition, driven by heterochronic shifts of dynamic genes, including transcriptional regulators with known roles in flowering. Thus, evolutionary diversity in Solanaceae inflorescence complexity is determined by subtle modifications of transcriptional programs during a critical transitional window of meristem maturation, which we propose underlies similar cases of plant architectural variation. More broadly, our findings parallel the recently described transcriptome "inverse hourglass" model for animal embryogenesis, suggesting both plant and animal morphological variation is guided by a mid-development period of transcriptome divergence.

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Section: Wwwgenomeorgmentioning

confidence: 88%

The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation

et al. 2016

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“…Limb bud development and the concomitant formation of limb skeletal structures are regulated by the intricate interplay and integration of various signaling pathways, with major roles played by the Shh, BMP, FGF, and Wnt/β-catenin pathways (reviewed for example in, Robert, 2007; Zuniga, 2015). The BMP signaling pathway is of pivotal importance especially for skeletal development.…”

Section: Introductionmentioning

confidence: 99%

A Novel Role for the BMP Antagonist Noggin in Sensitizing Cells to Non-canonical Wnt-5a/Ror2/Disheveled Pathway Activation

Bernatík

Radaszkiewicz

Běhal

et al. 2017

Front. Cell Dev. Biol.

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Mammalian limb development is driven by the integrative input from several signaling pathways; a failure to receive or a misinterpretation of these signals results in skeletal defects. The brachydactylies, a group of overlapping inherited human hand malformation syndromes, are mainly caused by mutations in BMP signaling pathway components. Two closely related forms, Brachydactyly type B2 (BDB2) and BDB1 are caused by mutations in the BMP antagonist Noggin (NOG) and the atypical receptor tyrosine kinase ROR2 that acts as a receptor in the non-canonical Wnt pathway. Genetic analysis of Nog and Ror2 functional interaction via crossing Noggin and Ror2 mutant mice revealed a widening of skeletal elements in compound but not in any of the single mutants, thus indicating genetic interaction. Since ROR2 is a non-canonical Wnt co-receptor specific for Wnt-5a we speculated that this phenotype might be a result of deregulated Wnt-5a signaling activation, which is known to be essential for limb skeletal elements growth and patterning. We show that Noggin potentiates activation of the Wnt-5a-Ror2-Disheveled (Dvl) pathway in mouse embryonic fibroblast (MEF) cells in a Ror2-dependent fashion. Rat chondrosarcoma chondrocytes (RCS), however, are not able to respond to Noggin in this fashion unless growth arrest is induced by FGF2. In summary, our data demonstrate genetic interaction between Noggin and Ror2 and show that Noggin can sensitize cells to Wnt-5a/Ror2-mediated non-canonical Wnt signaling, a feature that in cartilage may depend on the presence of active FGF signaling. These findings indicate an unappreciated function of Noggin that will help to understand BMP and Wnt/PCP signaling pathway interactions.

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“…These studies explain major skeletal differences in evolutionary distant species such as the absence of limbs in snakes. However, differences between the fore- and the hind-limb in the same species or skeletal differences observed among closely related tetrapods might be regulated in a different fashion, such as timing differences in the expression of signaling molecules (Richardson et al, 2009; Moore et al, 2015; Zuniga, 2015). …”

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confidence: 99%

Sox9 Expression in Amniotes: Species-Specific Differences in the Formation of Digits

Montero

Lorda‐Diez

Francisco-Morcillo

et al. 2017

Front. Cell Dev. Biol.

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In tetrapods the digit pattern has evolved to adapt to distinct locomotive strategies. The number of digits varies between species or even between hindlimb and forelimb within the same species. These facts illustrate the plasticity of embryonic limb autopods. Sox9 is a precocious marker of skeletal differentiation of limb mesenchymal cells. Its pattern of expression in the developing limb has been widely studied and reflects the activity of signaling cascades responsible for skeletogenesis. In this assay we stress previously overlooked differences in the pattern of expression of Sox9 in limbs of avian, mouse and turtle embryos which may reflect signaling differences associated with distinct limb skeletal morphologies observed in these species. Furthermore, we show that Sox9 gene expression is higher and maintained in the interdigital region in species with webbed digits in comparison with free digit animals.

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Next generation limb development and evolution: old questions, new perspectives

Cited by 126 publications

References 120 publications

The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation

The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation

A Novel Role for the BMP Antagonist Noggin in Sensitizing Cells to Non-canonical Wnt-5a/Ror2/Disheveled Pathway Activation

Sox9 Expression in Amniotes: Species-Specific Differences in the Formation of Digits

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