Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya

Abstract Background Carica papaya is a trioecious plant species with a genetic sex-determination system defined by sex chromosomes. Under unfavorable environmental conditions male and hermaphrodite exhibit sex-reversal. Previous genomic research revealed few candidate genes for sex differentiation i...

Full description

Bibliographic Details
Main Authors: Dessireé Zerpa-Catanho, Jennifer Wai, Ming Li Wang, Li’ang Yu, Julie Nguyen, Ray Ming
Format: Article
Language:English
Published: BMC 2019-12-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-019-2169-0
id doaj-37fcf58f7d6041c19fbf0c632908502a
record_format Article
spelling doaj-37fcf58f7d6041c19fbf0c632908502a2020-12-13T12:13:58ZengBMCBMC Plant Biology1471-22292019-12-0119112210.1186/s12870-019-2169-0Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papayaDessireé Zerpa-Catanho0Jennifer Wai1Ming Li Wang2Li’ang Yu3Julie Nguyen4Ray Ming5Department of Plant Biology, University of Illinois at Urbana-ChampaignDepartment of Plant Biology, University of Illinois at Urbana-ChampaignHawaii Agriculture Research CenterDepartment of Plant Biology, University of Illinois at Urbana-ChampaignDepartment of Plant Biology, University of Illinois at Urbana-ChampaignDepartment of Plant Biology, University of Illinois at Urbana-ChampaignAbstract Background Carica papaya is a trioecious plant species with a genetic sex-determination system defined by sex chromosomes. Under unfavorable environmental conditions male and hermaphrodite exhibit sex-reversal. Previous genomic research revealed few candidate genes for sex differentiation in this species. Nevertheless, more analysis is still needed to identify the mechanism responsible for sex flower organ development in papaya. Results The aim of this study was to identify differentially expressed genes among male, female and hermaphrodite flowers in papaya during early (pre-meiosis) and later (post-meiosis) stages of flower development. RNA-seq was used to evaluate the expression of differentially expressed genes and RT-qPCR was used to verify the results. Putative functions of these genes were analyzed based on their homology with orthologs in other plant species and their expression patterns. We identified a Male Sterility 1 gene (CpMS1) highly up-regulated in male and hermaphrodite flower buds compared to female flower buds, which expresses in small male flower buds (3–8 mm), and that might be playing an important role in male flower organ development due to its homology to MS1 genes previously identified in other plants. This is the first study in which the sex-biased expression of genes related to tapetum development in the anther developmental pathway is being reported in papaya. Besides important transcription factors related to flower organ development and flowering time regulation, we identified differential expression of genes that are known to participate in ABA, ROS and auxin signaling pathways (ABA-8-hydroxylases, AIL5, UPBEAT 1, VAN3-binding protein). Conclusions CpMS1 was expressed in papaya male and hermaphrodite flowers at early stages, suggesting that this gene might participate in male flower organ development processes, nevertheless, this gene cannot be considered a sex-determination gene. Due to its homology with other plant MS1 proteins and its expression pattern, we hypothesize that this gene participates in anther development processes, like tapetum and pollen development, downstream gender specification. Further gene functional characterization studies in papaya are required to confirm this hypothesis. The role of ABA and ROS signaling pathways in papaya flower development needs to be further explored as well.https://doi.org/10.1186/s12870-019-2169-0Carica papayaFlower developmentMale sterility geneRT-qPCRRNA-SeqSex differentiation
collection DOAJ
language English
format Article
sources DOAJ
author Dessireé Zerpa-Catanho
Jennifer Wai
Ming Li Wang
Li’ang Yu
Julie Nguyen
Ray Ming
spellingShingle Dessireé Zerpa-Catanho
Jennifer Wai
Ming Li Wang
Li’ang Yu
Julie Nguyen
Ray Ming
Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya
BMC Plant Biology
Carica papaya
Flower development
Male sterility gene
RT-qPCR
RNA-Seq
Sex differentiation
author_facet Dessireé Zerpa-Catanho
Jennifer Wai
Ming Li Wang
Li’ang Yu
Julie Nguyen
Ray Ming
author_sort Dessireé Zerpa-Catanho
title Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya
title_short Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya
title_full Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya
title_fullStr Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya
title_full_unstemmed Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya
title_sort differential gene expression among three sex types reveals a male sterility 1 (cpms1) for sex differentiation in papaya
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2019-12-01
description Abstract Background Carica papaya is a trioecious plant species with a genetic sex-determination system defined by sex chromosomes. Under unfavorable environmental conditions male and hermaphrodite exhibit sex-reversal. Previous genomic research revealed few candidate genes for sex differentiation in this species. Nevertheless, more analysis is still needed to identify the mechanism responsible for sex flower organ development in papaya. Results The aim of this study was to identify differentially expressed genes among male, female and hermaphrodite flowers in papaya during early (pre-meiosis) and later (post-meiosis) stages of flower development. RNA-seq was used to evaluate the expression of differentially expressed genes and RT-qPCR was used to verify the results. Putative functions of these genes were analyzed based on their homology with orthologs in other plant species and their expression patterns. We identified a Male Sterility 1 gene (CpMS1) highly up-regulated in male and hermaphrodite flower buds compared to female flower buds, which expresses in small male flower buds (3–8 mm), and that might be playing an important role in male flower organ development due to its homology to MS1 genes previously identified in other plants. This is the first study in which the sex-biased expression of genes related to tapetum development in the anther developmental pathway is being reported in papaya. Besides important transcription factors related to flower organ development and flowering time regulation, we identified differential expression of genes that are known to participate in ABA, ROS and auxin signaling pathways (ABA-8-hydroxylases, AIL5, UPBEAT 1, VAN3-binding protein). Conclusions CpMS1 was expressed in papaya male and hermaphrodite flowers at early stages, suggesting that this gene might participate in male flower organ development processes, nevertheless, this gene cannot be considered a sex-determination gene. Due to its homology with other plant MS1 proteins and its expression pattern, we hypothesize that this gene participates in anther development processes, like tapetum and pollen development, downstream gender specification. Further gene functional characterization studies in papaya are required to confirm this hypothesis. The role of ABA and ROS signaling pathways in papaya flower development needs to be further explored as well.
topic Carica papaya
Flower development
Male sterility gene
RT-qPCR
RNA-Seq
Sex differentiation
url https://doi.org/10.1186/s12870-019-2169-0
work_keys_str_mv AT dessireezerpacatanho differentialgeneexpressionamongthreesextypesrevealsamalesterility1cpms1forsexdifferentiationinpapaya
AT jenniferwai differentialgeneexpressionamongthreesextypesrevealsamalesterility1cpms1forsexdifferentiationinpapaya
AT mingliwang differentialgeneexpressionamongthreesextypesrevealsamalesterility1cpms1forsexdifferentiationinpapaya
AT liangyu differentialgeneexpressionamongthreesextypesrevealsamalesterility1cpms1forsexdifferentiationinpapaya
AT julienguyen differentialgeneexpressionamongthreesextypesrevealsamalesterility1cpms1forsexdifferentiationinpapaya
AT rayming differentialgeneexpressionamongthreesextypesrevealsamalesterility1cpms1forsexdifferentiationinpapaya
_version_ 1724385016186667008