Breaking the mold: understanding the evolution and development of lateral organs in diverse plant models

Walcher-Chevillet, Cristina L; Kramer, Elena M.

doi:10.1016/j.gde.2016.06.005

Cited by 17 publications

(11 citation statements)

References 58 publications

(58 reference statements)

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“…These processes have been described for leaves as largely sequential; during early development, cell division predominates, followed by a shift from cell division to cell expansion. The transition moves as a wave from one end of the organ to the other (Walcher-Chevillet & Kramer, 2016) and the arrest of cell division in leaves occurs before they are 10% of their final size (Lenhard & Czesnick, 2015). Far less is known about these processes in petal development in general and corolla tube development in particular.…”

Section: Discussionmentioning

confidence: 99%

Comparative analysis of corolla tube development across three closely related Mimulus species with different pollination syndromes

Gurung

Yuan

Diggle

2021

Evolution and Development

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Fusion of petals to form a corolla tube is considered a key innovation contributing to the diversification of many flowering plant lineages. Corolla tube length often varies dramatically among species and is a major determinant of pollinator preference. However, our understanding of the developmental dynamics underlying corolla tube length variation is very limited. Here we examined corolla tube growth in the Mimulus lewisii species complex, an emerging model system for studying the developmental genetics and evo‐devo of pollinator‐associated floral traits. We compared developmental and cellular processes associated with corolla tube length variation among the bee‐pollinated M. lewisii, the hummingbird‐pollinated Mimulus verbenaceus, and the self‐pollinated Mimulus parishii. We found that in all three species, cell size is non‐uniformly distributed along the mature tube, with the longest cells just distal to the stamen insertion site. Differences in corolla tube length among the three species are not associated with processes of organogenesis or early development but are associated with variation in multiple processes occurring later in development, including the location and duration of cell division and cell elongation. The tube growth curves of the small‐flowered M. parishii and large‐flowered M. lewisii are essentially indistinguishable, except that M. parishii tubes stop growing earlier at a smaller size, suggesting a critical role of heterochrony in the shift from outcrossing to selfing. These results not only highlight the developmental process associated with corolla tube variation among species but also provide a baseline reference for future developmental genetic analyses of mutants or transgenic plants with altered corolla tube morphology in this emerging model system.

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Section: Discussionmentioning

confidence: 99%

Comparative analysis of corolla tube development across three closely related Mimulus species with different pollination syndromes

Gurung

Yuan

Diggle

2021

Evolution and Development

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“…Unlike marginal elaboration, ventral elaboration refers to the formation of lips, scales, spurs, or other protruded structures on the ventral (i.e., abaxial) side of the petal (Endress and Matthews, 2006;Yao et al, 2019). The mechanisms underlying ventral elaboration are still unclear; yet, the data suggest that it may be related to the reactivation of the meristem program or rearrangement of the expression of adaxial/abaxial genes, or both (Walcher-Chevillet and Kramer, 2016). In Antirrhinum majus and Linaria vulgaris (Plantaginaceae), reactivation of the KNOXI genes, a key regulator of meristem development and maintenance, can cause the production of spur-like outgrowths on petals (Golz et al, 2002;Box et al, 2011).…”

Section: Mechanisms Underlying Marginal and Ventral Elaborationmentioning

confidence: 99%

“…In Arabidopsis (Arabidopsis thaliana; Brassicaceae) and many other petalous taxa (such as snapdragon [Antirrhinum majus], petunia [Petunia hybrida], columbine [Aquilegia], peonies [Paeonia], roses [Rosa], lilies [Lilium], and orchids [Orchidaceae]), petals, like any other types of lateral organs of plants, are formed through at least three highly conserved developmental processes: initiation, growth, and maturation. Genes, pathways, and networks involved in the proliferation, expansion, and differentiation of cells, as well as those specifying the adaxial-abaxial, proximal-distal, and lateral-medial polarities of the entire organ, are therefore indispensable (Irish, 2008;Huang and Irish, 2016;Walcher-Chevillet and Kramer, 2016;Shan et al, 2019). Yet, unlike many other types of lateral organs, petals are usually brightly colored and/or unusually shaped, suggesting that, in addition to the common themes of lateral organs, there are developmental processes that are specific to petals (such as determination of petal identity; generation of the sometimes highly specialized, three-dimensional structures; and/or formation of intriguing color patterns; Irish, 2008Irish, , 2017Huang and Irish, 2016;Moyroud and Glover, 2017).…”

Section: Introductionmentioning

confidence: 99%

Identification of the Key Regulatory Genes Involved in Elaborate Petal Development and Specialized Character Formation in Nigelladamascena (Ranunculaceae)

Zhang

Zhao

et al. 2020

Plant Cell

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Petals can be simple or elaborate, depending on whether they have lobes, teeth, fringes, or appendages along their margins, or possess spurs, scales, or other types of modifications on their adaxial/abaxial side, or both. Elaborate petals have been recorded in 23 orders of angiosperms and are generally believed to have played key roles in the adaptive evolution of corresponding lineages. The mechanisms underlying the formation of elaborate petals, however, are largely unclear. Here, by performing extensive transcriptomic and functional studies on Nigella damascena (Ranunculaceae), we explore the mechanisms underlying elaborate petal development and specialized character formation. In addition to the identification of genes and programs that are specifically/preferentially expressed in petals, we found genes and programs that are required for elaborate rather than simple petal development. By correlating the changes in gene expression with those in petal development, we identified 30 genes that are responsible for the marginal/ventral elaboration of petals and the initiation of several highly specialized morphological characters (e.g., pseudonectaries, long hairs, and short trichomes). Expression and functional analyses further confirmed that a class I homeodomain-leucine zipper family transcription factor gene, Nigella damascena LATE MERISTEM IDENTITY1 (NidaLMI1), plays important roles in the development of short trichomes and bifurcation of the lower lip. Our results not only provide the first portrait of elaborate petal development but also pave the way to understanding the mechanisms underlying lateral organ diversification in plants.

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“…At the cellular level, organogenesis consists of a sequence of three stages: the establishment of polarity, cell proliferation, and cell expansion ( Walcher-Chevillet and Kramer, 2016 ). The timing of initiation and termination of these stages is crucial for the size and shape of organs, and heterochrony in this sequence results in diversification of organ size and shape ( Figure 2 ).…”

Section: Mechanisms Driving Changes In Developmental Timing In Plantsmentioning

confidence: 99%

The Times They Are A-Changin’: Heterochrony in Plant Development and Evolution

Buendía-Monreal

Gillmor

2018

Front. Plant Sci.

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Alterations in the timing of developmental programs during evolution, that lead to changes in the shape, or size of organs, are known as heterochrony. Heterochrony has been widely studied in animals, but has often been neglected in plants. During plant evolution, heterochronic shifts have played a key role in the origin and diversification of leaves, roots, flowers, and fruits. Heterochrony that results in a juvenile or simpler outcome is known as paedomorphosis, while an adult or more complex outcome is called peramorphosis. Mechanisms that alter developmental timing at the cellular level affect cell proliferation or differentiation, while those acting at the tissue or organismal level change endogenous aging pathways, morphogen signaling, and metabolism. We believe that wider consideration of heterochrony in the context of evolution will contribute to a better understanding of plant development.

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Breaking the mold: understanding the evolution and development of lateral organs in diverse plant models

Cited by 17 publications

References 58 publications

Comparative analysis of corolla tube development across three closely related Mimulus species with different pollination syndromes

Comparative analysis of corolla tube development across three closely related Mimulus species with different pollination syndromes

Identification of the Key Regulatory Genes Involved in Elaborate Petal Development and Specialized Character Formation in Nigelladamascena (Ranunculaceae)

The Times They Are A-Changin’: Heterochrony in Plant Development and Evolution

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