Pan-European study of genotypes and phenotypes in the Arabidopsis relative Cardamine hirsuta reveals how adaptation, demography, and development shape diversity patterns

Baumgarten, Lukas; Pieper, Bjorn; Song, Baoxing; Mane, Sébastien; Lempe, Janne; Lamb, Jonathan; Cooke, Elizabeth L.; Srivastava, Rachita; Strütt, Stefan; Žanko, Danijela; Casimiro, Pedro GP; Hallab, Asis; Cartolano, Maria; Tattersall, Alexander D.; Huettel, Bruno; Filatov, Dmitry A.; Pavlidis, Pavlos; Neuffer, Barbara; Bazakos, Christos; Schaefer, Hanno; Mott, Richard; Gan, Xiangchao; Alonso-Blanco, Carlos; Laurent, Stefan; Tsiantis, Miltos

doi:10.1371/journal.pbio.3002191

Cited by 13 publications

(6 citation statements)

References 143 publications

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“…Notably, natural allelic variation in ChSPL9 underlies a heterochronic QTL (quantitative trait locus) that contributed to the evolution of a distinctive C. hirsuta morphotype prevalent in the Azorean islands. 41 This QTL shows evidence for positive selection, and its distribution mirrors a climate gradient that broadly shaped the Azorean flora. 41 Taken together, the effects of SPL9 in leaf shape diversity, combined with genetic analyses of heteroblasty and its natural variation in different land plants including trees, 11,[41][42][43][44][45][46][47][48][49][50][51] indicate that the heterochronic regulation of growth that we report here constrained plant evolution at both the micro-and macroevolutionary scales.…”

Section: Discussionmentioning

confidence: 92%

“…The C. hirsuta chspl9 mutant was created using CRISPR-Cas9 technology. 41 It contains two single-base insertions within the first exon of ChSPL9 , with a guanine (G) inserted after the 53 rd base of the coding sequence (CDS), causing a reading frame shift and a premature stop codon 15-bp afterwards, and a cytosine (C) inserted after the 179 th base of the CDS. A Cleaved Amplified Polymorphic Sequences (CAPS) marker was developed to genotype chspl9 allele (see Table S1).…”

Section: Methods Detailsmentioning

confidence: 99%

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Age-associated growth control modifies leaf proximodistal symmetry and enables leaf shape diversification

Li,

Jenke,

Strauss

et al. 2024

Preprint

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Biological shape diversity is often manifested in modulation of organ symmetry and modification of the patterned elaboration of repeated shape elements.1-5 Whether and how these two aspects of shape determination are coordinately regulated is unclear.5-7 Plant leaves provide an attractive system to investigate this problem, because they usually show asymmetries along their proximodistal axis, along which they can also produce repeated marginal outgrowths such as serrations or leaflets.1 One case of leaf shape diversity is heteroblasty, where the leaf form in a single genotype is modified with progressive plant age.8-11 In Arabidopsis thaliana, a plant with simple leaves, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE9 (SPL9) controls heteroblasty by activating CyclinD3 expression, thereby sustaining proliferative growth and retarding differentiation in adult leaves.12 However, the precise significance of SPL9 action for leaf symmetry and marginal patterning is unknown. By combining genetics, quantitative shape analyses, and time-lapse imaging, we show that, in A. thaliana, proximodistal symmetry of the leaf blade decreases in response to an age-dependent SPL9 expression gradient, and that SPL9 action coordinately regulates the distribution and shape of marginal serrations and overall leaf form. Using comparative analyses, we demonstrate that heteroblastic growth reprogramming in Cardamine hirsuta, a complex-leafed relative of A. thaliana, also involves prolonging the duration of cell proliferation and delaying differentiation. We further provide evidence that SPL9 enables species-specific action of homeobox genes that promote leaf complexity. In conclusion, we identify an age-dependent layer of organ proximodistal growth regulation that modulates leaf symmetry and has enabled leaf shape diversification.

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Section: Discussionmentioning

confidence: 92%

Section: Methods Detailsmentioning

confidence: 99%

Age-associated growth control modifies leaf proximodistal symmetry and enables leaf shape diversification

Li,

Jenke,

Strauss

et al. 2024

Preprint

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“…FRI alleles are associated with flowering time plasticity in regions experiencing high annual temperature variation ( Fournier-Level et al 2022 ), which may be related to its temperature-sensitive properties ( Zhu et al 2021 ). The evolutionary relevance of FRI variation extends to Cardamine hirsuta , where 3 distinct FRI loss-of-function alleles associate with early flowering ( Baumgarten et al 2023 ).…”

Section: Natural Variation Has Identified Critical Nodes Driving Flow...mentioning

confidence: 99%

Flowering time: From physiology, through genetics to mechanism

Maple,

Zhu,

Hepworth

et al. 2024

Plant Physiology

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Plant species have evolved different requirements for environmental/endogenous cues to induce flowering. Originally, these varying requirements were thought to reflect the action of different molecular mechanisms. Thinking changed when genetic and molecular analysis in Arabidopsis thaliana revealed that a network of environmental and endogenous signalling input pathways converge to regulate a common set of ‘floral pathway integrators’. Variation in the predominance of the different input pathways within a network can generate the diversity of requirements observed in different species. Many genes identified by flowering time mutants were found to encode general developmental and gene regulators, with their targets having a specific flowering function. Studies of natural variation in flowering were more successful at identifying genes acting as nodes in the network central to adaptation and domestication. Attention has now turned to mechanistic dissection of flowering time gene function and how that has changed during adaptation. This will inform breeding strategies for climate-proof crops and help define which genes act as critical flowering nodes in many other species.

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“…Comparative approaches extend the reach of developmental genetics by developing new tools in less well-studied species. For example, Cardamine hirsuta is a relative of Arabidopsis with many divergent traits and genetic tools to study them (Hay & Tsiantis, 2006; Hay et al ., 2014; Vlad et al ., 2014; Monniaux et al ., 2018; Baumgarten et al ., 2023). Explosive seed dispersal is one such trait that distinguishes C. hirsuta from Arabidopsis.…”

Section: Introductionmentioning

confidence: 99%

Amphicarpic development in the emerging model organismCardamine chenopodiifolia

Emonet,

Pérez-Antón,

Neumann

et al. 2024

Preprint

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- Amphicarpy is an unusual trait where two fruit types develop: one above and the other below ground. This trait is not found in conventional model species, therefore, its development and molecular genetics remain under-studied. Here, we establish Cardamine chenopodiifolia as an emerging experimental system to study amphicarpy. - We characterized the development of C. chenopodiifolia, focusing on differences in morphology and cell wall histochemistry between above- and below-ground fruit. We generated a reference transcriptome using PacBio full-length transcript sequencing (IsoSeq) and used a combination of short and long read sequencing to analyse differential gene expression between above- and below-ground fruit valves. - C. chenopodiifolia has two contrasting modes of seed dispersal. The main shoot fails to bolt and initiates floral primordia that bury underground where they self-pollinate and set seed. By contrast, axillary shoots bolt to position flowers and exploding seed pods above ground. Morphological differences between aerial explosive fruit and subterranean non-explosive fruit were reflected in a large number of differentially regulated genes involved in photosynthesis, secondary cell wall formation and defence responses. - Tools established in C. chenopodiifolia, such as a reference transcriptome, draft genome assembly and stable plant transformation, pave the way to explore under-studied traits and discover new biological mechanisms.

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Pan-European study of genotypes and phenotypes in the Arabidopsis relative Cardamine hirsuta reveals how adaptation, demography, and development shape diversity patterns

Cited by 13 publications

References 143 publications

Age-associated growth control modifies leaf proximodistal symmetry and enables leaf shape diversification

Age-associated growth control modifies leaf proximodistal symmetry and enables leaf shape diversification

Flowering time: From physiology, through genetics to mechanism

Amphicarpic development in the emerging model organismCardamine chenopodiifolia

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