Multifunctional evolution of B and AGL6 MADS box genes in orchids

Hsu, Hsing‐Fun; Chen, Wei-Han; Shen, Yi-Hsuan; Hsu, Wu Huei; Mao, Wan-Ting; Yang, Chang‐Hsien

doi:10.1038/s41467-021-21229-w

Cited by 42 publications

(37 citation statements)

References 55 publications

(69 reference statements)

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“…The former is specifically expressed and exclusively required for labellum formation and reported as L‐code mode in orchids. The latter is reported as the P‐code of perianth development to specify the sepal/petal previously (Hsu et al ., 2015a , 2021 , 2015b , 2015a , 2021 , 2015b ). Among these expanded clades, we originally found that one of the four gene copies in SEP clade, CsSEP4 , was ectopically expressed in the gynostemium of the wild‐type flower and expended to all floral organs of a gynostemium‐like perianth variant.…”

Section: Resultsmentioning

confidence: 99%

The genome of Cymbidium sinense revealed the evolution of orchid traits

Yang

Gao

Wei

et al. 2021

Plant Biotechnology Journal

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Summary The Orchidaceae is of economic and ecological importance and constitutes ˜10% of all seed plant species. Here, we report a genome physical map for Cymbidium sinense, a well‐known species belonging to genus Cymbidium that has thousands of natural variation varieties of flower organs, flower and leaf colours and also referred as the King of Fragrance, which make it arose into a unique cultural symbol in China. The high‐quality chromosome‐scale genome assembly was 3.52 Gb in size, 29 638 protein‐coding genes were predicted, and evidence for whole‐genome duplication shared with other orchids was provided. Marked amplification of cytochrome‐ and photosystem‐related genes was observed, which was consistent with the shade tolerance and dark green leaves of C. sinense. Extensive duplication of MADS‐box genes, and the resulting subfunctional and expressional differentiation, was associated with regulation of species‐specific flower traits, including wild‐type and mutant‐type floral patterning, seasonal flowering and ecological adaption. CsSEP4 was originally found to positively regulate gynostemium development. The CsSVP genes and their interaction proteins CsAP1 and CsSOC1 were significantly expanded and involved in the regulation of low‐temperature‐dependent flowering. Important genetic clues to the colourful leaf traits, purple‐black flowers and volatile trait in C. sinense were also found. The results provide new insights into the molecular mechanisms of important phenotypic traits of Cymbidium and its evolution and serve as a powerful platform for future evolutionary studies and molecular breeding of orchids.

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Section: Resultsmentioning

confidence: 99%

The genome of Cymbidium sinense revealed the evolution of orchid traits

Yang

Gao

Wei

et al. 2021

Plant Biotechnology Journal

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“…Members of the R2R3-MYB, bHLH, and WD-Repeat proteins, including those that we have briefly highlighted in this study, are prime candidates given that they are key determinants of anthocyanin pigmentation intensity and also patterning in many flowers ( Davies et al, 2012 ; Wessinger and Rausher, 2012 ). However, MADS-box transcription factors should also be investigated as some are involved in establishing proper floral organ identity programs, photosynthesis, chlorophyll metabolism, and pigmentation in orchids ( Pan et al, 2014 ; Hsu et al, 2021 ). The integration of various omics approaches (e.g., large-scale transcriptomic, metabolomic, ionomics) is also anticipated to provide a holistic view of how structural genes, regulatory factors, and cellular constituents (e.g., pigments, metal ions, pH) interact and mediate the evolutionary color transitions between sexually deceptive systems.…”

Section: Discussionmentioning

confidence: 99%

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

2022

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Sexually deceptive plants secure pollination by luring specific male insects as pollinators using a combination of olfactory, visual, and morphological mimicry. Flower color is a key component to this attraction, but its chemical and genetic basis remains poorly understood. Chiloglottis trapeziformis is a sexually deceptive orchid which has predominantly dull green-red flowers except for the central black callus projecting from the labellum lamina. The callus mimics the female of the pollinator and the stark color contrast between the black callus and dull green or red lamina is thought to enhance the visibility of the mimic. The goal of this study was to investigate the chemical composition and genetic regulation of temporal and spatial color patterns leading to visual mimicry, by integrating targeted metabolite profiling and transcriptomic analysis. Even at the very young bud stage, high levels of anthocyanins were detected in the dark callus, with peak accumulation by the mature bud stage. In contrast, anthocyanin levels in the lamina peaked as the buds opened and became reddish-green. Coordinated upregulation of multiple genes, including dihydroflavonol reductase and leucoanthocyanidin dioxygenase, and the downregulation of flavonol synthase genes (FLS) in the callus at the very young bud stage underpins the initial high anthocyanin levels. Conversely, within the lamina, upregulated FLS genes promote flavonol glycoside over anthocyanin production, with the downstream upregulation of flavonoid O-methyltransferase genes further contributing to the accumulation of methylated flavonol glycosides, whose levels peaked in the mature bud stage. Finally, the peak anthocyanin content of the reddish-green lamina of the open flower is underpinned by small increases in gene expression levels and/or differential upregulation in the lamina in select anthocyanin genes while FLS patterns showed little change. Differential expression of candidate genes involved in specific transport, vacuolar acidification, and photosynthetic pathways may also assist in maintaining the distinct callus and contrasting lamina color from the earliest bud stage through to the mature flower. Our findings highlight that flower color in this sexually deceptive orchid is achieved by complex tissue-specific coordinated regulation of genes and biochemical pathways across multiple developmental stages.

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“…Therefore, we analyzed the relationships among CmAP3, CmUIF1, and CmPI, which belongs to the class B GLOBOSA/PISTILLATA subfamily of MADS-box TFs ( Fig. S11 ) and has been reported to interact with AP3 to determine the organ identity of petals and stamens [ 21 , 61 ]. The results showed that CmAP3 was not able to interact with CmUIF1 ( Fig.…”

Section: Discussionmentioning

confidence: 99%

“…CYC2c and CYC2g determined the position and zygomorphy of ray florets [ 68 ]. CYC2d was shown to repress the growth of stamens and dorsal corolla lobes [ 61 , 62 ]. In general, research on the regulatory mechanism of CYC2 -like genes has focused mainly on protein–protein interactions [ 70 , 71 ], whereas the regulatory networks upstream of these genes are poorly understood.…”

Section: Discussionmentioning

confidence: 99%

The transcription factor complex CmAP3-CmPI-CmUIF1 modulates carotenoid metabolism by directly regulating the carotenogenic gene CmCCD4a-2 in chrysanthemum

Deng

et al. 2022

Horticulture Research

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Carotenoids are one of the most important pigments for the coloring in many plants, fruits and flowers. Recently, significant progress has been made in carotenoid metabolism. However, the specific understanding on transcriptional regulation controlling the expression of carotenoid metabolic genes remains extremely limited. Anemone-type chrysanthemum, as a special group of chrysanthemum cultivars, contain elongated disc florets in capitulum, which usually appear in different colors compared with the ray florets since accumulating distinct content of carotenoids. In this study, the carotenoid composition and content of the ray and disc florets of an anemone-type chrysanthemum cultivar ‘Dong Li Fen Gui’ were analyzed by high-performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS) and the key structural gene CmCCD4a-2, of which differential expression resulted in the distinct content of carotenoids accumulated in these two types of florets, was identified. Then the promoter sequence of CmCCD4a-2 was used as bait to screen a chrysanthemum flower cDNA library and two transcription factors, CmAP3 and CmUIF1 were identified. Y2H, BiFC and Y3H experiments demonstrated that these two TFs were connected by CmPI to form CmAP3-CmPI-CmUIF1 TF complex. This TF complex regulated carotenoid metabolism through activating the expression of CmCCD4a-2 directly. Furthermore, a large number of target genes regulated directly by the CmAP3-CmPI-CmUIF1 TF complex, including carotenoid biosynthetic genes, flavonoid biosynthetic genes and flower development-related genes, were identified by DNA-affinity purification sequencing (DAP-seq), which indicated that the CmAP3-CmPI-CmUIF1 TF complex might participate in multiple processes. These findings expand our knowledge for the transcriptional regulation of carotenoid metabolism in plants and will be helpful to manipulating carotenoid accumulation in chrysanthemum.

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Multifunctional evolution of B and AGL6 MADS box genes in orchids

Cited by 42 publications

References 55 publications

The genome of Cymbidium sinense revealed the evolution of orchid traits

The genome of Cymbidium sinense revealed the evolution of orchid traits

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

The transcription factor complex CmAP3-CmPI-CmUIF1 modulates carotenoid metabolism by directly regulating the carotenogenic gene CmCCD4a-2 in chrysanthemum

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