De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification

Abstract Background Coccinia grandis (ivy gourd), is a dioecious member of Cucurbitaceae having heteromorphic sex chromosomes. Chromosome constitution of male and female plants of C. grandis is 22A + XY and 22A + XX respectively. Earlier we showed that a unique gynomonoecious form of C. grandis (22A...

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Main Authors: Ravi Suresh Devani, Sangram Sinha, Jayeeta Banerjee, Rabindra Kumar Sinha, Abdelhafid Bendahmane, Anjan Kumar Banerjee
Format: Article
Language:English
Published: BMC 2017-12-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-017-1187-z
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author Ravi Suresh Devani
Sangram Sinha
Jayeeta Banerjee
Rabindra Kumar Sinha
Abdelhafid Bendahmane
Anjan Kumar Banerjee
author_facet Ravi Suresh Devani
Sangram Sinha
Jayeeta Banerjee
Rabindra Kumar Sinha
Abdelhafid Bendahmane
Anjan Kumar Banerjee
author_sort Ravi Suresh Devani
collection DOAJ
description Abstract Background Coccinia grandis (ivy gourd), is a dioecious member of Cucurbitaceae having heteromorphic sex chromosomes. Chromosome constitution of male and female plants of C. grandis is 22A + XY and 22A + XX respectively. Earlier we showed that a unique gynomonoecious form of C. grandis (22A + XX) also exists in nature bearing morphologically hermaphrodite flowers (GyM-H). Additionally, application of silver nitrate (AgNO3) on female plants induces stamen development leading to the formation of morphologically hermaphrodite flowers (Ag-H) despite the absence of Y-chromosome. Due to the unavailability of genome sequence and the slow pace at which sex-linked genes are identified, sex expression and modification in C. grandis are not well understood. Results We have carried out a comprehensive RNA-Seq study from early-staged male, female, GyM-H, and Ag-H as well as middle-staged male and GyM-H flower buds. A de novo transcriptome was assembled using Trinity and annotated by BLAST2GO and Trinotate pipelines. The assembled transcriptome consisted of 467,233 ‘Trinity Transcripts’ clustering into 378,860 ‘Trinity Genes’. Female_Early_vs_Male_Early, Ag_Early_vs_Female_Early, and GyM-H_Middle_vs_Male_Middle comparisons exhibited 35,694, 3574, and 14,954 differentially expressed transcripts respectively. Further, qRT-PCR analysis of selected candidate genes validated digital gene expression profiling results. Interestingly, ethylene response-related genes were found to be upregulated in female buds compared to male buds. Also, we observed that AgNO3 treatment suppressed ethylene responses in Ag-H flowers by downregulation of ethylene-responsive transcription factors leading to stamen development. Further, GO terms related to stamen development were enriched in early-staged male, GyM-H, and Ag-H buds compared to female buds supporting the fact that stamen growth gets arrested in female flowers. Conclusions Suppression of ethylene responses in both male and Ag-H compared to female buds suggests a probable role of ethylene in stamen suppression similar to monoecious cucurbits such as melon and cucumber. Also, pollen fertility associated GO terms were depleted in middle-staged GyM-H buds compared to male buds indicating the necessity of Y-chromosome for pollen fertility. Overall, this study would enable identification of new sex-biased genes for further investigation of stamen arrest, pollen fertility, and AgNO3-mediated sex modification.
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spelling doaj.art-28ef127024c14bc6b606a68b16847d1c2022-12-22T02:42:46ZengBMCBMC Plant Biology1471-22292017-12-0117111510.1186/s12870-017-1187-zDe novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modificationRavi Suresh Devani0Sangram Sinha1Jayeeta Banerjee2Rabindra Kumar Sinha3Abdelhafid Bendahmane4Anjan Kumar Banerjee5Biology Division, Indian Institute of Science Education and Research (IISER)Department of Botany, Tripura UniversityBiology Division, Indian Institute of Science Education and Research (IISER)Department of Botany, Tripura UniversityIPS2, INRA, CNRS, University Paris Sud, University of Evry, University Paris Diderot, University of Paris SaclayBiology Division, Indian Institute of Science Education and Research (IISER)Abstract Background Coccinia grandis (ivy gourd), is a dioecious member of Cucurbitaceae having heteromorphic sex chromosomes. Chromosome constitution of male and female plants of C. grandis is 22A + XY and 22A + XX respectively. Earlier we showed that a unique gynomonoecious form of C. grandis (22A + XX) also exists in nature bearing morphologically hermaphrodite flowers (GyM-H). Additionally, application of silver nitrate (AgNO3) on female plants induces stamen development leading to the formation of morphologically hermaphrodite flowers (Ag-H) despite the absence of Y-chromosome. Due to the unavailability of genome sequence and the slow pace at which sex-linked genes are identified, sex expression and modification in C. grandis are not well understood. Results We have carried out a comprehensive RNA-Seq study from early-staged male, female, GyM-H, and Ag-H as well as middle-staged male and GyM-H flower buds. A de novo transcriptome was assembled using Trinity and annotated by BLAST2GO and Trinotate pipelines. The assembled transcriptome consisted of 467,233 ‘Trinity Transcripts’ clustering into 378,860 ‘Trinity Genes’. Female_Early_vs_Male_Early, Ag_Early_vs_Female_Early, and GyM-H_Middle_vs_Male_Middle comparisons exhibited 35,694, 3574, and 14,954 differentially expressed transcripts respectively. Further, qRT-PCR analysis of selected candidate genes validated digital gene expression profiling results. Interestingly, ethylene response-related genes were found to be upregulated in female buds compared to male buds. Also, we observed that AgNO3 treatment suppressed ethylene responses in Ag-H flowers by downregulation of ethylene-responsive transcription factors leading to stamen development. Further, GO terms related to stamen development were enriched in early-staged male, GyM-H, and Ag-H buds compared to female buds supporting the fact that stamen growth gets arrested in female flowers. Conclusions Suppression of ethylene responses in both male and Ag-H compared to female buds suggests a probable role of ethylene in stamen suppression similar to monoecious cucurbits such as melon and cucumber. Also, pollen fertility associated GO terms were depleted in middle-staged GyM-H buds compared to male buds indicating the necessity of Y-chromosome for pollen fertility. Overall, this study would enable identification of new sex-biased genes for further investigation of stamen arrest, pollen fertility, and AgNO3-mediated sex modification.http://link.springer.com/article/10.1186/s12870-017-1187-zCoccinia grandisDioeciousGynomonoeciousDe novo transcriptomeStamen arrestSilver nitrate
spellingShingle Ravi Suresh Devani
Sangram Sinha
Jayeeta Banerjee
Rabindra Kumar Sinha
Abdelhafid Bendahmane
Anjan Kumar Banerjee
De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification
BMC Plant Biology
Coccinia grandis
Dioecious
Gynomonoecious
De novo transcriptome
Stamen arrest
Silver nitrate
title De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification
title_full De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification
title_fullStr De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification
title_full_unstemmed De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification
title_short De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification
title_sort de novo transcriptome assembly from flower buds of dioecious gynomonoecious and chemically masculinized female coccinia grandis reveals genes associated with sex expression and modification
topic Coccinia grandis
Dioecious
Gynomonoecious
De novo transcriptome
Stamen arrest
Silver nitrate
url http://link.springer.com/article/10.1186/s12870-017-1187-z
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