Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandis

Abstract Background Dioecy is an important sexual system wherein, male and female flowers are borne on separate unisexual plants. Knowledge of sex-related differences can enhance our understanding in molecular and developmental processes leading to unisexual flower development. Coccinia grandis is a...

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Main Authors: Ravi Suresh Devani, Tejas Chirmade, Sangram Sinha, Abdelhafid Bendahmane, Bhushan B. Dholakia, Anjan Kumar Banerjee, Jayeeta Banerjee
Format: Article
Language:English
Published: BMC 2019-07-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-019-1937-1
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author Ravi Suresh Devani
Tejas Chirmade
Sangram Sinha
Abdelhafid Bendahmane
Bhushan B. Dholakia
Anjan Kumar Banerjee
Jayeeta Banerjee
author_facet Ravi Suresh Devani
Tejas Chirmade
Sangram Sinha
Abdelhafid Bendahmane
Bhushan B. Dholakia
Anjan Kumar Banerjee
Jayeeta Banerjee
author_sort Ravi Suresh Devani
collection DOAJ
description Abstract Background Dioecy is an important sexual system wherein, male and female flowers are borne on separate unisexual plants. Knowledge of sex-related differences can enhance our understanding in molecular and developmental processes leading to unisexual flower development. Coccinia grandis is a dioecious species belonging to Cucurbitaceae, a family well-known for diverse sexual forms. Male and female plants have 22A + XY and 22A + XX chromosomes, respectively. Previously, we have reported a gynomonoecious form (22A + XX) of C. grandis bearing morphologically hermaphrodite flowers (GyM-H) and female flowers (GyM-F). Also, we have showed that foliar spray of AgNO3 on female plant induces morphologically hermaphrodite bud development (Ag-H) despite the absence of Y-chromosome. Results To identify sex-related differences, total proteomes from male, female, GyM-H and Ag-H flower buds at early and middle stages of development were analysed by label-free proteomics. Protein search against the cucumber protein sequences (Phytozome) as well as in silico translated C. grandis flower bud transcriptome database, resulted in the identification of 2426 and 3385 proteins (FDR ≤ 1%), respectively. The latter database was chosen for further analysis as it led to the detection of higher number of proteins. Identified proteins were annotated using BLAST2GO pipeline. SWATH-MS-based comparative abundance analysis between Female_Early_vs_Male_Early, Ag_Early_vs_Female_Early, GyM-H_Middle_vs_Male_Middle and Ag_Middle_vs_ Male_Middle led to the identification of 650, 1108, 905 and 805 differentially expressed proteins, respectively, at fold change ≥1.5 and P ≤ 0.05. Ethylene biosynthesis-related candidates as highlighted in protein interaction network were upregulated in female buds compared to male buds. AgNO3 treatment on female plant induced proteins related to pollen development in Ag-H buds. Additionally, a few proteins governing pollen germination and tube growth were highly enriched in male buds compared to Ag-H and GyM-H buds. Conclusion Overall, current proteomic analysis provides insights in the identification of key proteins governing dioecy and unisexual flower development in cucurbitaceae, the second largest horticultural family in terms of economic importance. Also, our results suggest that the ethylene-mediated stamen inhibition might be conserved in dioecious C. grandis similar to its monoecious cucurbit relatives. Further, male-biased proteins associated with pollen germination and tube growth identified here can help in understanding pollen fertility.
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spelling doaj.art-3d128729d7be4cdfaa7328f98157a6572022-12-22T00:06:42ZengBMCBMC Plant Biology1471-22292019-07-0119111510.1186/s12870-019-1937-1Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandisRavi Suresh Devani0Tejas Chirmade1Sangram Sinha2Abdelhafid Bendahmane3Bhushan B. Dholakia4Anjan Kumar Banerjee5Jayeeta Banerjee6Biology Division, Indian Institute of Science Education and Research (IISER)Biochemical Science Division National Chemical laboratory (CSIR-NCL)Department of Botany, Tripura UniversityIPS2, INRA, CNRS, University Paris Sud, University of Evry, University of Paris Diderot, University of Paris SaclayBiology Division, Indian Institute of Science Education and Research (IISER)Biology Division, Indian Institute of Science Education and Research (IISER)Biology Division, Indian Institute of Science Education and Research (IISER)Abstract Background Dioecy is an important sexual system wherein, male and female flowers are borne on separate unisexual plants. Knowledge of sex-related differences can enhance our understanding in molecular and developmental processes leading to unisexual flower development. Coccinia grandis is a dioecious species belonging to Cucurbitaceae, a family well-known for diverse sexual forms. Male and female plants have 22A + XY and 22A + XX chromosomes, respectively. Previously, we have reported a gynomonoecious form (22A + XX) of C. grandis bearing morphologically hermaphrodite flowers (GyM-H) and female flowers (GyM-F). Also, we have showed that foliar spray of AgNO3 on female plant induces morphologically hermaphrodite bud development (Ag-H) despite the absence of Y-chromosome. Results To identify sex-related differences, total proteomes from male, female, GyM-H and Ag-H flower buds at early and middle stages of development were analysed by label-free proteomics. Protein search against the cucumber protein sequences (Phytozome) as well as in silico translated C. grandis flower bud transcriptome database, resulted in the identification of 2426 and 3385 proteins (FDR ≤ 1%), respectively. The latter database was chosen for further analysis as it led to the detection of higher number of proteins. Identified proteins were annotated using BLAST2GO pipeline. SWATH-MS-based comparative abundance analysis between Female_Early_vs_Male_Early, Ag_Early_vs_Female_Early, GyM-H_Middle_vs_Male_Middle and Ag_Middle_vs_ Male_Middle led to the identification of 650, 1108, 905 and 805 differentially expressed proteins, respectively, at fold change ≥1.5 and P ≤ 0.05. Ethylene biosynthesis-related candidates as highlighted in protein interaction network were upregulated in female buds compared to male buds. AgNO3 treatment on female plant induced proteins related to pollen development in Ag-H buds. Additionally, a few proteins governing pollen germination and tube growth were highly enriched in male buds compared to Ag-H and GyM-H buds. Conclusion Overall, current proteomic analysis provides insights in the identification of key proteins governing dioecy and unisexual flower development in cucurbitaceae, the second largest horticultural family in terms of economic importance. Also, our results suggest that the ethylene-mediated stamen inhibition might be conserved in dioecious C. grandis similar to its monoecious cucurbit relatives. Further, male-biased proteins associated with pollen germination and tube growth identified here can help in understanding pollen fertility.http://link.springer.com/article/10.1186/s12870-019-1937-1Coccinia grandisDioecySex modificationStamen arrestPollen fertilityProteomics
spellingShingle Ravi Suresh Devani
Tejas Chirmade
Sangram Sinha
Abdelhafid Bendahmane
Bhushan B. Dholakia
Anjan Kumar Banerjee
Jayeeta Banerjee
Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandis
BMC Plant Biology
Coccinia grandis
Dioecy
Sex modification
Stamen arrest
Pollen fertility
Proteomics
title Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandis
title_full Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandis
title_fullStr Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandis
title_full_unstemmed Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandis
title_short Flower bud proteome reveals modulation of sex-biased proteins potentially associated with sex expression and modification in dioecious Coccinia grandis
title_sort flower bud proteome reveals modulation of sex biased proteins potentially associated with sex expression and modification in dioecious coccinia grandis
topic Coccinia grandis
Dioecy
Sex modification
Stamen arrest
Pollen fertility
Proteomics
url http://link.springer.com/article/10.1186/s12870-019-1937-1
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