scholarly journals Co-expression clustering across flower development identifies modules for diverse floral forms in Achimenes (Gesneriaceae)

PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e8778 ◽  
Author(s):  
Wade R. Roberts ◽  
Eric H. Roalson

Background Genetic pathways involved with flower color and shape are thought to play an important role in the development of flowers associated with different pollination syndromes, such as those associated with bee, butterfly, or hummingbird pollination. Because pollination syndromes are complex traits that are orchestrated by multiple genes and pathways, the gene regulatory networks have not been explored. Gene co-expression networks provide a systems level approach to identify important contributors to floral diversification. Methods RNA-sequencing was used to assay gene expression across two stages of flower development (an early bud and an intermediate stage) in 10 species of Achimenes (Gesneriaceae). Two stage-specific co-expression networks were created from 9,503 orthologs and analyzed to identify module hubs and the network periphery. Module association with bee, butterfly, and hummingbird pollination syndromes was tested using phylogenetic mixed models. The relationship between network connectivity and evolutionary rates (dN/dS) was tested using linear models. Results Networks contained 65 and 62 modules that were largely preserved between developmental stages and contained few stage-specific modules. Over a third of the modules in both networks were associated with flower color, shape, and pollination syndrome. Within these modules, several hub nodes were identified that related to the production of anthocyanin and carotenoid pigments and the development of flower shape. Evolutionary rates were decreased in highly connected genes and elevated in peripheral genes. Discussion This study aids in the understanding of the genetic architecture and network properties underlying the development of floral form and provides valuable candidate modules and genes for future studies.

2019 ◽  
Author(s):  
Wade R Roberts ◽  
Eric H Roalson

AbstractBackgroundGenetic pathways involved with flower color and shape are thought to play an important role in the development of flowers associated with different pollination syndromes, such as those associated with bee, butterfly, or hummingbird pollination. Because pollination syndromes are complex traits that are orchestrated by multiple genes and pathways, the gene networks have not been explored. Gene co-expression networks provide a systems level approach to identify important contributors to floral diversification.MethodsRNA-sequencing was used to assay gene expression across two stages of flower development (an early bud and an intermediate stage) in 10 species of Achimenes (Gesneriaceae). Two stage-specific co-expression networks were created from 9503 orthologs and analyzed to identify module hubs and the network periphery. Module association with bee, butterfly, and hummingbird pollination syndromes was tested using phylogenetic mixed models. The relationship between network connectivity and evolutionary rates (dN/dS) was tested using linear models.ResultsNetworks contained 65 and 62 modules that were largely preserved between developmental stages and contained few stage-specific modules. Over a third of the modules in both networks were associated with flower color, shape, and pollination syndrome. Within these modules, several hub nodes were identified that related to the production of anthocyanin and carotenoid pigments and the development of flower shape. Evolutionary rates were decreased in highly connected genes and elevated in peripheral genes.DiscussionThis study aids in the understanding of the genetic architecture and network properties underlying the development of floral form and provides valuable candidate modules and genes for future studies.


2020 ◽  
Vol 11 ◽  
Author(s):  
Ezgi Ogutcen ◽  
Karine Durand ◽  
Marina Wolowski ◽  
Laura Clavijo ◽  
Catherine Graham ◽  
...  

Changes in floral pigmentation can have dramatic effects on angiosperm evolution by making flowers either attractive or inconspicuous to different pollinator groups. Flower color largely depends on the type and abundance of pigments produced in the petals, but it is still unclear whether similar color signals rely on same biosynthetic pathways and to which extent the activation of certain pathways influences the course of floral color evolution. To address these questions, we investigated the physical and chemical aspects of floral color in the Neotropical Gesnerioideae (ca. 1,200 spp.), in which two types of anthocyanins, hydroxyanthocyanins, and deoxyanthocyanins, have been recorded as floral pigments. Using spectrophotometry, we measured flower reflectance for over 150 species representing different clades and pollination syndromes. We analyzed these reflectance data to estimate how the Gesnerioideae flowers are perceived by bees and hummingbirds using the visual system models of these pollinators. Floral anthocyanins were further identified using high performance liquid chromatography coupled to mass spectrometry. We found that orange/red floral colors in Gesnerioideae are produced either by deoxyanthocyanins (e.g., apigenidin, luteolinidin) or hydroxyanthocyanins (e.g., pelargonidin). The presence of deoxyanthocyanins in several lineages suggests that the activation of the deoxyanthocyanin pathway has evolved multiple times in the Gesnerioideae. The hydroxyanthocyanin-producing flowers span a wide range of colors, which enables them to be discriminated by hummingbirds or bees. By contrast, color diversity among the deoxyanthocyanin-producing species is lower and mainly represented at longer wavelengths, which is in line with the hue discrimination optima for hummingbirds. These results indicate that Gesnerioideae have evolved two different biochemical mechanisms to generate orange/red flowers, which is associated with hummingbird pollination. Our findings also suggest that the activation of the deoxyanthocyanin pathway has restricted flower color diversification to orange/red hues, supporting the potential constraining role of this alternative biosynthetic pathway on the evolutionary outcome of phenotypical and ecological diversification.


2020 ◽  
Author(s):  
Hui-Rong Duan ◽  
Li-Rong Wang ◽  
Guang-Xin Cui ◽  
Xue-Hui Zhou ◽  
Xiao-Rong Duan ◽  
...  

Abstract Background: To understand the gene expression networks controlling flower color formation in alfalfa, flowers anthocyanins were identified using two materials with contrasting flower colors, namely Defu and Zhongtian No. 3, and transcriptome analyses of PacBio full-length sequencing combined with RNA sequencing were performed, across four flower developmental stages. Results: Malvidin and petunidin glycoside derivatives were the major anthocyanins in the flowers of Defu, which were lacking in the flowers of Zhongtian No. 3. The two transcriptomic datasets provided a comprehensive and systems-level view on the dynamic gene expression networks underpinning alfalfa flower color formation. By weighted gene coexpression network analyses, we identified candidate genes and hub genes from the modules closely related to floral developmental stages. PAL , 4CL , CHS , CHR , F3’H , DFR , and UFGT were enriched in the important modules. Additionally, PAL6 , PAL9 , 4CL18 , CHS2 , 4 and 8 were identified as hub genes. Thus, a hypothesis explaining the lack of purple color in the flower of Zhongtian No. 3 was proposed. Conclusions: These analyses identified a large number of potential key regulators controlling flower color pigmentation, thereby providing new insights into the molecular networks underlying alfalfa flower development.


2019 ◽  
Author(s):  
Hui-Rong Duan ◽  
Li-Rong Wang ◽  
Guang-Xin Cui ◽  
Xue-Hui Zhou ◽  
Xiao-Rong Duan ◽  
...  

Abstract Background: To understand the gene expression networks controlling flower color formation in alfalfa, transcriptome analyses of PacBio full-length sequencing combined with RNA sequencing were performed using two materials with contrasting flower colors, namely Defu and Zhongtian No. 3, across four flower developmental stages. Results: The two datasets provided a comprehensive and systems-level view on the dynamic gene expression networks underpinning alfalfa flower color formation. By weighted gene coexpression network analyses, we identified candidate genes and hub genes from the modules closely related to floral developmental stages. PAL, 4CL, CHS, CHR, F3’H, DFR, and UFGT were enriched in the important modules. Additionally, PAL6, PAL9, 4CL18, CHS2, 4 and 8 were identified as hub genes. Thus, a hypothesis explaining the lack of purple color in the flower of Zhongtian No. 3 was proposed. Conclusions: These analyses identified a large number of potential key regulators controlling flower color pigmentation, thereby providing new insights into the molecular networks underlying alfalfa flower development.


2020 ◽  
Author(s):  
Hui-Rong Duan ◽  
Li-Rong Wang ◽  
Guang-Xin Cui ◽  
Xue-Hui Zhou ◽  
Xiao-Rong Duan ◽  
...  

Abstract Background: To understand the gene expression networks controlling flower color formation in alfalfa, flowers anthocyanins were identified using two materials with contrasting flower colors, namely Defu and Zhongtian No. 3, and transcriptome analyses of PacBio full-length sequencing combined with RNA sequencing were performed, across four flower developmental stages. Results: Malvidin and petunidin glycoside derivatives were the major anthocyanins in the flowers of Defu, which were lacking in the flowers of Zhongtian No. 3. The two transcriptomic datasets provided a comprehensive and systems-level view on the dynamic gene expression networks underpinning alfalfa flower color formation. By weighted gene coexpression network analyses, we identified candidate genes and hub genes from the modules closely related to floral developmental stages. PAL, 4CL, CHS, CHR, F3’H, DFR, and UFGT were enriched in the important modules. Additionally, PAL6, PAL9, 4CL18, CHS2, 4 and 8 were identified as hub genes. Thus, a hypothesis explaining the lack of purple color in the flower of Zhongtian No. 3 was proposed. Conclusions: These analyses identified a large number of potential key regulators controlling flower color pigmentation, thereby providing new insights into the molecular networks underlying alfalfa flower development.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3636 ◽  
Author(s):  
Lucía Salas-Arcos ◽  
Carlos Lara ◽  
Juan Francisco Ornelas

Background In many plant species, pollination syndromes predict the most effective pollinator. However, other floral visitors may also offer effective pollination services and promote mixed pollination systems. Several species of the species-rich Penstemon (Plantaginaceae) exhibit a suite of floral traits that suggest adaptation for pollination by both hymenopterans and hummingbirds. Transitions from the ancestral hymenopteran pollination syndrome to more derived hummingbird pollination syndrome may be promoted if the quantity or quality of visits by hummingbirds is increased and if the ancestral pollinator group performs less efficiently. The quantification of such shifts in pollination systems in the group is still limited. We aimed to investigate floral traits linked to this pollination syndrome in Penstemon gentianoides with flowers visited by bumblebees and hummingbirds. Methods We investigated the floral biology, pollinator assemblages, breeding system and nectar production patterns ofP. gentianoides inhabiting a temperate montane forest in central Mexico. Pollination experiments were also conducted to assess the pollinator effectiveness of bumblebees and hummingbirds. Results P. gentianoides flowers are protandrous, with 8-d male phase (staminate) flowers, followed by the ∼1–7 d female phase (pistillate phase). Flowers display traits associated with hymenopteran pollination, including purple flowers abruptly ampliate-ventricose to a broad throat with anthers and stigmas included, and long lifespans. However, the nectar available in the morning hours was abundant and dilute, traits linked to flowers with a hummingbird pollination syndrome. Two hummingbird species made most of the visits to flowers, Selasphorus platycercus (30.3% of all visits), followed by Archilochus colubris (11.3%). Bumblebees (Bombus ephippiatus, B. huntii and B. weisi) accounted for 51.8% of all recorded visits, but their foraging activity was restricted to the warmer hours. Hummingbirds made more foraging bouts and visited more flowers than hymenopteran species. Flowers experimentally pollinated by B. ephippiatus produced significantly more fruits than those pollinated by S. platycercus. However, there was no statistical difference in the number of seeds produced per fruit when a bumblebee or a hummingbird was the pollinator. Conclusions We have shown that bumblebees and hummingbirds visit and pollinate P. gentianoides flowers. Despite floral traits resembling the hymenoptera pollination syndrome, flowers of P. gentianoides offer characteristic nectar rewards to flowers with a hummingbird pollination syndrome. Although pollination efficiency is higher among flowers visited by hymenoptera, the noteworthy percentage of fruit production and number of seeds per fruit derived from hummingbird pollination highlights the importance of hummingbirds as a functional group of pollinators that might have potential evolutionary consequences to the plants.


2014 ◽  
Vol 369 (1648) ◽  
pp. 20130349 ◽  
Author(s):  
Carolyn A. Wessinger ◽  
Lena C. Hileman ◽  
Mark D. Rausher

Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes—bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus . In an F 2 mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.


2020 ◽  
Author(s):  
Hui-Rong Duan ◽  
Li-Rong Wang ◽  
Guang-Xin Cui ◽  
Xue-Hui Zhou ◽  
Xiao-Rong Duan ◽  
...  

Abstract Background: To understand the gene expression networks controlling flower color formation in alfalfa, flowers anthocyanins were identified using two materials with contrasting flower colors, namely Defu and Zhongtian No. 3, and transcriptome analyses of PacBio full-length sequencing combined with RNA sequencing were performed, across four flower developmental stages. Results: Malvidin and petunidin glycoside derivatives were the major anthocyanins in the flowers of Defu, which were lacking in the flowers of Zhongtian No. 3. The two transcriptomic datasets provided a comprehensive and systems-level view on the dynamic gene expression networks underpinning alfalfa flower color formation. By weighted gene coexpression network analyses, we identified candidate genes and hub genes from the modules closely related to floral developmental stages. PAL , 4CL , CHS , CHR , F3’H , DFR , and UFGT were enriched in the important modules. Additionally, PAL6 , PAL9 , 4CL18 , CHS2 , 4 and 8 were identified as hub genes. Thus, a hypothesis explaining the lack of purple color in the flower of Zhongtian No. 3 was proposed. Conclusions: These analyses identified a large number of potential key regulators controlling flower color pigmentation, thereby providing new insights into the molecular networks underlying alfalfa flower development.


Biomolecules ◽  
2021 ◽  
Vol 11 (2) ◽  
pp. 248
Author(s):  
Chang Ha Park ◽  
Hyeon Ji Yeo ◽  
Ye Jin Kim ◽  
Bao Van Nguyen ◽  
Ye Eun Park ◽  
...  

This study aimed to elucidate the variations in primary and secondary metabolites during Lycorisradiata flower development using high performance liquid chromatography (HPLC) and gas chromatography time-of-flight mass spectrometry (GC-TOFMS). The result showed that seven carotenoids, seven phenolic acids, three anthocyanins, and galantamine were identified in the L. radiata flowers. Most secondary metabolite levels gradually decreased according to the flower developmental stages. A total of 51 metabolites, including amines, sugars, sugar intermediates, sugar alcohols, amino acids, organic acids, phenolic acids, and tricarboxylic acid (TCA) cycle intermediates, were identified and quantified using GC-TOFMS. Among the hydrophilic compounds, most amino acids increased during flower development; in contrast, TCA cycle intermediates and sugars decreased. In particular, glutamine, asparagine, glutamic acid, and aspartic acid, which represent the main inter- and intracellular nitrogen carriers, were positively correlated with the other amino acids and were negatively correlated with the TCA cycle intermediates. Furthermore, quantitation data of the 51 hydrophilic compounds were subjected to partial least-squares discriminant analyses (PLS-DA) to assess significant differences in the metabolites of L. radiata flowers from stages 1 to 4. Therefore, this study will serve as the foundation for a biochemical approach to understand both primary and secondary metabolism in L. radiata flower development.


2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Yu Qiao ◽  
Qiming Cheng ◽  
Yutong Zhang ◽  
Wei Yan ◽  
Fengyan Yi ◽  
...  

Abstract Background Sainfoin (Onobrychis viciifolia Scop) is not only a high-quality legume forage, but also a nectar-producing plant. Therefore, the flower color of sainfoin is an important agronomic trait, but the factors affecting its flower phenotype are still unclear. To gain insights into the regulatory networks associated with metabolic pathways of coloration compounds (flavonoids or anthocyanins) and identify the key genes, we conducted a comprehensive analysis of the phenotype, metabolome and transcriptome of WF and AF of sainfoin. Results Delphinidin, petunidin and malvidin derivatives were the main anthocyanin compounds in the AF of sainfoin. These substances were not detected in the WF of sainfoin. The transcriptomes of WF and AF in sainfoin at the S1 and S3 stages were obtained using the Illumina HiSeq4000 platform. Overall, 10,166 (4273 upregulated and 5893 downregulated) and 15,334 (8174 upregulated and 7160 downregulated) DEGs were identified in flowers at S1 and S3 stages, respectively (WF-VS-AF). KEGG pathway annotations showed that 6396 unigenes were annotated to 120 pathways and contained 866 DEGs at S1 stages, and 6396 unigenes were annotated to 131 pathways and included 1546 DEGs at the S3 stage. Nine DEGs belonging to the “flavonoid biosynthesis”and “phenylpropanoid biosynthesis” pathways involved in flower color formation were identified and verified by RT-qPCR analyses. Among these DEGs, 4CL3, FLS, ANS, CHS, DFR and CHI2 exhibited downregulated expression, and F3H exhibited upregulated expression in the WF compared to the AF, resulting in a decrease in anthocyanin synthesis and the formation of WF in sainfoin. Conclusions This study is the first to use transcriptome technology to study the mechanism of white flower formation in sainfoin. Our transcriptome data will be a great enrichment of the genetic information for sainfoin. In addition, the data presented herein will provide valuable molecular information for genetic breeding and provide insight into the future study of flower color polymorphisms in sainfoin.


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