Evolution of carnivorous traps from planar leaves through simple shifts in gene expression

Whitewoods, Christopher D.; Gonçalves, Beatriz; Cheng, Jie; Cui, Min-Long; Kennaway, Richard; Lee, Karen; Bushell, Claire; Yu, Min; Piao, Chunlan; Coen, Enrico

doi:10.1126/science.aay5433

Cited by 95 publications

(98 citation statements)

References 34 publications

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“…Consequently, shifts from the gametophyte to the sporophyte program would only require changes in expression of a relatively small set of major genes. This is in line with multiple studies reporting how shifts in temporal or local expression of a small set of genes can lead to radical change in morphology (Frankel et al, 2011;Ichihashi et al, 2014;Sicard et al, 2014;Di Ruocco et al, 2018;Whitewoods et al, 2020). Whether this assertion may also apply to the molecular mechanisms underlying contrasting sporophytic architectures is discussed in the paragraphs below.…”

Section: Proportion Of Preferentially Sporophyte-expressed Genes Is Ssupporting

confidence: 80%

Transcriptional Landscapes of Divergent Sporophyte Development in Two Mosses, Physcomitrium (Physcomitrella) patens and Funaria hygrometrica

et al. 2020

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Understanding the molecular basis of morphological shifts is a fundamental question of evolutionary biology. New morphologies may arise through the birth/death of genes (gene gain/loss) or by reutilizing existing gene sets. Yet, the relative contribution of these two processes to radical morphological shifts is still poorly understood. Here, we use the model system of two mosses, Funaria hygrometrica and Physcomitrium (Physcomitrella) patens, to investigate the molecular mechanisms underlying contrasting sporophyte architectures. We used comparative analysis of time-series expression data for four stages of sporophyte development in both species to address this question in detail. We found that large-scale differences in sporophytic architecture are mainly governed by orthologous (i.e., shared) genes frequently experiencing temporal gene expression shifts between the two species. While the absolute number of species-specific genes expressed during sporophyte development is somewhat smaller, we observed a significant increase of their proportion in preferentially sporophyte expressed genes, suggesting a fundamental role in the sporophyte phase. However, further functional studies are necessary to determine their contribution to diverging sporophyte morphologies. Our results add to the growing set of studies suggesting that radical changes in morphology may rely on the heterochronic expression of conserved regulators.

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Section: Proportion Of Preferentially Sporophyte-expressed Genes Is Ssupporting

confidence: 80%

Transcriptional Landscapes of Divergent Sporophyte Development in Two Mosses, Physcomitrium (Physcomitrella) patens and Funaria hygrometrica

et al. 2020

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“…The pictures in Fig. 3s were generated by using GFtbox (http://sourceforge.net/projects/gftbox) with two coordinated networks: the Polarity Regulatory Network and Growth Rates Regulatory Network 61,62 . The initial state was a mesh which consists of 36,000 finite elements with a grid showing the deformation.…”

Section: Discussionmentioning

confidence: 99%

The morphology, molecular development and ecological function of pseudonectaries on Nigella damascena (Ranunculaceae) petals

Liao

Zhao

et al. 2020

Nat Commun

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Pseudonectaries, or false nectaries, the glistening structures that resemble nectaries or nectar droplets but do not secrete nectar, show considerable diversity and play important roles in plant-animal interactions. The morphological nature, optical features, molecular underpinnings and ecological functions of pseudonectaries, however, remain largely unclear. Here, we show that pseudonectaries of Nigella damascena (Ranunculaceae) are tiny, regional protrusions covered by tightly arranged, non-secretory polygonal epidermal cells with flat, smooth and reflective surface, and are clearly visible even under ultraviolet light and bee vision. We also show that genes associated with cell division, chloroplast development and wax formation are preferably expressed in pseudonectaries. Specifically, NidaYABBY5, an abaxial gene with ectopic expression in pseudonectaries, is indispensable for pseudonectary development: knockdown of it led to complete losses of pseudonectaries. Notably, when flowers without pseudonectaries were arrayed beside those with pseudonectaries, clear differences were observed in the visiting frequency, probing time and visiting behavior of pollinators (i.e., honey bees), suggesting that pseudonectaries serve as both visual attractants and nectar guides.

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“…Note While this work was being prepared for publication another group reported a transformation protocol for U. gibba using solid media [45,46]. Our work uses an alternative system in liquid media that leads to rapid recovery and propagation of transformed plants.…”

Section: Discussionmentioning

confidence: 99%

Agrobacterium tumefaciens mediated transformation of the aquatic carnivorous plant Utricularia gibba

2020

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Background: The genus Utricularia belongs to Lentibulariaceae, the largest family of carnivorous plants, which includes terrestrial, epiphytic and aquatic species. The development of specialized structures that evolved for carnivory is a feature of this genus that has been of great interest to biologists since Darwin's early studies. Utricularia gibba is itself an aquatic plant with sophisticated bladder traps having one of the most complex suction mechanisms for trapping prey. However, the molecular characterization of the mechanisms that regulate trap development and the biophysical processes involved in prey trapping are still largely unknown due to the lack of a simple and reproducible gene transfer system. Results:Here, we report the establishment of a simple, fast and reproducible protocol for genetic transformation of U. gibba based on the T-DNA of Agrobacterium tumefaciens. An in vitro selection system using Phosphinotricin as a selective agent was established for U. gibba. Plant transformation was confirmed by histochemical GUS assays and PCR and qRT-PCR analyses. We report on the expression pattern of the 35S promoter and of the promoter of a trapspecific ribonuclease gene in transgenic U. gibba plants. Conclusions:The genetic transformation protocol reported here is an effective method for studying developmental biology and functional genomics of this genus of carnivorous plants and advances the utility of U. gibba as a model system to study developmental processes involved in trap formation.

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Evolution of carnivorous traps from planar leaves through simple shifts in gene expression

Cited by 95 publications

References 34 publications

Transcriptional Landscapes of Divergent Sporophyte Development in Two Mosses, Physcomitrium (Physcomitrella) patens and Funaria hygrometrica

Transcriptional Landscapes of Divergent Sporophyte Development in Two Mosses, Physcomitrium (Physcomitrella) patens and Funaria hygrometrica

The morphology, molecular development and ecological function of pseudonectaries on Nigella damascena (Ranunculaceae) petals

Agrobacterium tumefaciens mediated transformation of the aquatic carnivorous plant Utricularia gibba

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