The cellular basis for synergy between RCO and KNOX1 homeobox genes in leaf shape diversity

Wang, Yi; Strauss, Soeren; Liu, Shanda; Pieper, Bjorn; Lymbouridou, Rena; Runions, Adam; Tsiantis, Miltos

doi:10.1016/j.cub.2022.08.020

Cited by 25 publications

(19 citation statements)

References 62 publications

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“…Why would these genes be predisposed to regulating morphological change? We propose that GT1 and VRS1 occupy a conserved position within the genetic network that allows them to regulate morphological characters without a high level of pleiotropy, and thus they may be more likely to gain and retain new roles within development (Martin & Orgogozo, 2013; Stern & Orgogozo, 2009; Uller et al, 2018; Wang et al, 2022). The capacity of these genes to repress growth across diverse species also supports this idea (Fig.…”

Section: Discussionmentioning

confidence: 99%

Duplicate transcription factorsGT1andVRS1regulate branching and fertile flower number in maize andBrachypodium distachyon

Gallagher

Man

Chiaramida

et al. 2023

Preprint

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Crop engineering and de novo domestication using genome editing are new frontiers in agriculture. However, outside of well-studied crops and model systems, prioritizing engineering targets remains challenging. Evolution can serve as our guide, revealing high-priority genes with deeply conserved roles. Indeed,GRASSY TILLERS1(GT1),SIX-ROWED SPIKE1(VRS1), and their homologs have repeatedly been targets of selection in domestication and evolution. This repeated selection may be because these genes have an ancient, conserved role in regulating growth repression. To test this, we determined the roles ofGT1andVRS1homologs in maize (Zea mays) and the distantly related grass brachypodium (Brachypodium distachyon) using CRISPR-Cas9 gene editing and mutant analysis.GT1andVRS1have roles in floral development in maize and barley, respectively. Grass flowers are borne in branching structures called spikelets. In maize spikelets, carpels are suppressed in half of all initiated ear flowers. These spikelets can only produce single grains. We show thatgt1; vrs1-like1(vrl1) mutants have derepressed carpels in ear flowers. Importantly, these plants can produce two grains per spikelet. In brachypodium,bdgt1; bdvrl1mutants have more branches, spikelets, and flowers than wildtype plants, indicating conserved roles forGT1andVRS1homologs in growth suppression. Indeed, maizeGT1can suppress growth inArabidopsis thaliana, separated from the grasses by ca. 160 million years of evolution. Thus,GT1andVRS1maintain their potency as growth regulators across vast timescales and in distinct developmental contexts. Modulating the activity of these and other conserved genes may be critical in crop engineering.

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Section: Discussionmentioning

confidence: 99%

Duplicate transcription factorsGT1andVRS1regulate branching and fertile flower number in maize andBrachypodium distachyon

Gallagher

Man

Chiaramida

et al. 2023

Preprint

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“…26,28–37 To this end, we took advantage of the fact that KNOX1 and RCO genes are sufficient to increase leaf complexity when ectopically expressed in A. thaliana leaves. 17,38,39 We found that they create lobes or leaflets in adult (leaf8) but not juvenile leaves (leaf1) of A. thaliana (Figure 4A), despite discernible expression in both (Figures 4B-4D’) - which is also the case in the C. hirsuta endogenous context (Figures 4E-4F’). These observations indicate that the adult developmental context is an essential prerequisite for these two homeobox genes to increase leaf complexity.…”

Section: Resultsmentioning

confidence: 79%

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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“…To further investigate how PAVs affect fruit quality traits in pears, we identified genes showing significant differences in PAV occurrence frequency between Asian and European pear populations that are functionally associated with fruit shape, aroma, color, stone cells, and fruit hardness. In total, we identified 192 fruit quality traits associated genes ( Table S18 ), with homologous six genes exhibiting significant correlations with fruit shape development, including transcription repressor gene OFP16 ( PsbM011G02493 and PsbM005G03117 ) (Snouffer et al, 2020), homeobox protein knotted-1-like gene KNOX1 ( Pco_Presence_Seq_006877 ) (Wang et al, 2022), SUN domain-containing protein 5 gene ( Pdr_Presence_Seq_013651 ) (Ma et al, 2022), and TRM (PsbM003G00721 and Pco_Presence_Seq_003059 ) (Zhang et al, 2023). For example, the gene PsbM005G03117 is present in all Asian pear accessions but less than half of European pear accessions (Occurency frequency: 0.55) (Differential occurrence frequency: 0.45, P-value: 1.54E-08), while PsbM011G02493 showing a different pattern than present in all European pear accessions and near three-quarters of Asian pear accessions (Occurrency frequency: 0.72) (Differential occurrence frequency: 0.28, P-value: 1.06E-05).…”

Section: Resultsmentioning

confidence: 99%

Pan-genome of pear provides insights into the fruit quality traits differentiation between Asian and European pears

Ding,

Hu,

Liu

et al. 2023

Preprint

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The pear (Pyrus spp.) is a remarkable fruit, well known for its diverse flavors, textures, culinary versatility, and global horticultural importance. However, the genetic diversity responsible for its extensive phenotypic variations remains largely unexplored. Here, wede novoassembled and annotated the genomes of the maternal (PsbM) and paternal (PsbF) lines of the hybrid ‘Yuluxiang’ pear and constructed the first pear pangenome of 1.15Gb by combining these two genomes with five previously published pear genomes. Using the constructed pangenome, we identified 21,224 gene PAVs and 1,158,812 SNPs in the non-reference genome that were absent in the PsbM reference genome. Compared with SNP markers, we found that PAV-based analysis provides additional insights into the pear population structure. In addition, we also revealed that some genes associated with pear fruit quality traits have differential occurrence frequencies and differential gene expression between Asian and European populations. Moreover, our analysis of the pear pangenome revealed a mutated SNP and an insertion in the promoter region of the genePsbMGH3.1potentially enhances sepal shedding in ‘Xuehuali’ which is vital for pear quality. This research helps further capture the genetic diversity of pear populations and provides valuable genomic resources for accelerating pear breeding.

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The cellular basis for synergy between RCO and KNOX1 homeobox genes in leaf shape diversity

Cited by 25 publications

References 62 publications

Duplicate transcription factorsGT1andVRS1regulate branching and fertile flower number in maize andBrachypodium distachyon

Duplicate transcription factorsGT1andVRS1regulate branching and fertile flower number in maize andBrachypodium distachyon

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

Pan-genome of pear provides insights into the fruit quality traits differentiation between Asian and European pears

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