Dynamic evolution of small signalling peptide compensation in plant stem cell control

Kwon, Choon Tak; Tang, Lingli; Wang, Xingang; Gentile, Iacopo; Hendelman, Anat; Robitaille, Gina; Eck, Joyce Van; Cao, Xu; Lippman, Zachary B.

doi:10.1038/s41477-022-01118-w

Cited by 30 publications

(40 citation statements)

References 72 publications

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“…These findings may help fuel more integrative genetic and evolution investigations of homoeologous exchange, subgenome expression dominance, and duplicate gene evolution that can leverage the vast new output of genomes with ancestral and recent polyploidy and explicit evolutionary models of ancestral subenomes (Emery et al 2018; Hao et al 2021,2022; Parey et al 2022). This new avenue of investigation may help further examine evolution and epistasis as well as selection and divergence among paralogs (Qi et al 2021; Conover and Wendel, 2022; Kwon et al 2022), and spur further integration of methods and data across phylogenomics, comparative and population genomics, and network biology (Renny-Byfield et al 2017; Blischak et al 2018). Such work can enhance plant breeding efforts by providing a strengthened evolutionary understanding of the consequences of gene duplications, gene balance, and subgenome dominance (Rodriguez-Leal et al 2017; Bird et al 2018; Salman-Minkov et al 2016; Turner-Hissong et al 2020; Bayer et al 2021; Bomblies 2022).…”

Section: Discussionmentioning

confidence: 99%

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

Bird

Pires

VanBuren

et al. 2021

Preprint

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Allopolyploidy involves the hybridization of two evolutionary diverged species and the doubling of genomic material. Frequently, allopolyploids exhibit genomic rearrangements that recombine, duplicate, or delete homoeologous regions of the newly formed genome. While decades of investigation have focused on how genome duplication leads to systematic differences in the retention and expression of duplicate genes, the impact of genomic rearrangements on genome evolution has received less attention. We used genomic and transcriptomic data for six independently resynthesized, isogenic Brassica napus lines in the first, fifth, and tenth generation to identify genomic rearrangements and assess their impact on gene expression dynamics related to subgenome dominance and gene dosage constraint. We find that dosage constraints on the gene expression response to polyploidy begin to loosen within the first ten generations of evolution and systematically differ between dominant and non-dominant subgenomes. We also show that genomic rearrangements can bias estimation of homoeolog expression bias, but fail to fully obscure which subgenome is dominantly expressed. Finally, we demonstrate that dosage-sensitive genes exhibit the same kind of coordinated response to homoeologous exchange as they do for genome duplication, suggesting constraint on dosage balance also acts on these changes to gene dosage.

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Section: Discussionmentioning

confidence: 99%

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

Bird

Pires

VanBuren

et al. 2021

Preprint

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“…RNA-seq and differentially expressed genes (DEGs) analyses were performed as previously described with slight modification ( Kwon et al, 2022 ). Briefly, the libraries for RNA-seq were prepared by the KAPA mRNA HyperPrep Kit (Roche, Basel, Switzerland).…”

Section: Methodsmentioning

confidence: 99%

“…We developed efficient Agrobacterium -mediated transformation and CRISPR–Cas9 genome editing in the diploid groundcherry species P. grisea , and demonstrated the utility of these tools by mutating orthologs of tomato domestication genes in groundcherry to improve productivity traits ( Lemmon et al, 2018 ; Swartwood and van Eck, 2019 ). More recently, P. grisea was critical in revealing pleiotropic functions of an ancient homeobox gene, and in dissecting the evolution of redundancy between duplicated signaling peptide genes controlling stem cell proliferation in the Solanaceae ( Hendelman et al, 2021 ; Kwon et al, 2022 ). However, high-quality reference genomes of P. grisea and other species have been lacking, and are needed to promote the full potential and deployment of this system as has been achieved in tomato.…”

Section: Introductionmentioning

confidence: 99%

Establishing Physalis as a Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome

Alonge

Ramakrishnan

et al. 2022

The Plant Cell

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The highly diverse Solanaceae family contains several widely studied model and crop species. Fully exploring, appreciating, and exploiting this diversity requires additional model systems. Particularly promising are orphan fruit crops in the genus Physalis, which occupy a key evolutionary position in the Solanaceae and capture understudied variation in traits such as inflorescence complexity, fruit ripening and metabolites, disease and insect resistance, self-compatibility, and most notable, the striking inflated calyx syndrome (ICS), an evolutionary novelty found across angiosperms where sepals grow exceptionally large to encapsulate fruits in a protective husk. We recently developed transformation and genome editing in Physalis grisea (groundcherry). However, to systematically explore and unlock the potential of this and related Physalis as genetic systems, high-quality genome assemblies are needed. Here, we present chromosome-scale references for P. grisea and its close relative P. pruinosa and use these resources to study natural and engineered variation in floral traits. We first rapidly identified a natural structural variant in a bHLH gene that causes petal color variation. Further, and against expectations, we found that CRISPR-Cas9 targeted mutagenesis of 11 MADS-box genes, including purported essential regulators of ICS, had no effect on inflation. In a forward genetics screen, we identified huskless, which lacks ICS due to mutation of an AP2-like gene that causes sepals and petals to merge into a single whorl of mixed identity. These resources and findings elevate Physalis to a new Solanaceae model system, and establish a paradigm in the search for factors driving ICS.

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“…RNA-seq and differentially expressed genes analyses were performed as previously described with slight modification (Kwon et al, 2022). Briefly, the libraries for RNA-seq were prepared by the KAPA mRNA HyperPrep Kit (Roche).…”

Section: Transcriptome Analysis Of Huskless and Wtmentioning

confidence: 99%

“…We developed efficient Agrobacterium-mediated transformation and CRISPR-Cas9 genome editing in the diploid groundcherry species P. grisea, and demonstrated the utility of these tools by mutating orthologs of tomato domestication genes in groundcherry to improve productivity traits (Lemmon et al, 2018;Swartwood & Van Eck, 2019) . More recently, P. grisea was critical in revealing pleiotropic functions of an ancient homeobox gene, and in dissecting evolution of redundancy between duplicated signaling peptide genes controlling stem cell proliferation in the Solanaceae (Hendelman et al, 2021;Kwon et al, 2022) . However, high-quality reference genomes of P. grisea and other species have been lacking, and are needed to promote the full potential and deployment of this system as has been achieved in tomato.…”

Section: Introductionmentioning

confidence: 99%

Establishing Physalis as a new Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome

Alonge

Ramakrishnan

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

The highly diverse Solanaceae family contains several widely studied model and crop species. Fully exploring, appreciating, and exploiting this diversity requires additional model systems. Particularly promising are orphan fruit crops in the genus Physalis, which occupy a key evolutionary position in the Solanaceae and capture understudied variation in traits such as inflorescence complexity, fruit ripening and metabolites, disease and insect resistance, self-compatibility, and most notable, the striking Inflated Calyx Syndrome (ICS), an evolutionary novelty found across angiosperms where sepals grow exceptionally large to encapsulate fruits in a protective husk. We recently developed transformation and genome editing in Physalis grisea (groundcherry). However, to systematically explore and unlock the potential of this and related Physalis as genetic systems, high-quality genome assemblies are needed. Here, we present chromosome-scale references for P. grisea and its close relative P. pruinosa and use these resources to study natural and engineered variation in floral traits. We first rapidly identified a natural structural variant in a bHLH gene that causes petal color variation. Further, and against expectations, we found that CRISPR-Cas9 targeted mutagenesis of 11 MADS-box genes, including purported essential regulators of ICS, had no effect on inflation. In a forward genetics screen, we identified huskless, which lacks ICS due to mutation of an AP2-like gene that causes sepals and petals to merge into a single whorl of mixed identity. These resources and findings elevate Physalis to a new Solanaceae model system, and establish a new paradigm for the search of factors driving ICS.

show abstract

Dynamic evolution of small signalling peptide compensation in plant stem cell control

Cited by 30 publications

References 72 publications

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

Establishing Physalis as a Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome

Establishing Physalis as a new Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome

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