Comparative Transcriptome Analysis of Male and Female Flowers in Spinacia Oleracea L

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2020 Dec 1

PMID 33256615

Citations 11

Authors

Ning Li

Ziwei Meng

Minjie Tao

Yueyuan Wang

Yulan Zhang

Shufen Li

Wujun Gao

Chuanliang Deng

Affiliations

Soon will be listed here.

Abstract

Background: Dioecious spinach (Spinacia oleracea L.), a commercial and nutritional vegetable crop, serves as a model for studying the mechanisms of sex determination and differentiation in plants. However, this mechanism is still unclear. Herein, based on PacBio Iso-seq and Illumina RNA-seq data, comparative transcriptome analysis of male and female flowers were performed to explore the sex differentiation mechanism in spinach.

Results: Compared with published genome of spinach, 10,800 transcripts were newly annotated; alternative splicing, alternative polyadenylation and lncRNA were analyzed for the first time, increasing the diversity of spinach transcriptome. A total of 2965 differentially expressed genes were identified between female and male flowers at three early development stages. The differential expression of RNA splicing-related genes, polyadenylation-related genes and lncRNAs suggested the involvement of alternative splicing, alternative polyadenylation and lncRNA in sex differentiation. Moreover, 1946 male-biased genes and 961 female-biased genes were found and several candidate genes related to gender development were identified, providing new clues to reveal the mechanism of sex differentiation. In addition, weighted gene co-expression network analysis showed that auxin and gibberellin were the common crucial factors in regulating female or male flower development; however, the closely co-expressed genes of these two factors were different between male and female flower, which may result in spinach sex differentiation.

Conclusions: In this study, 10,800 transcripts were newly annotated, and the alternative splicing, alternative polyadenylation and long-noncoding RNA were comprehensively analyzed for the first time in spinach, providing valuable information for functional genome study. Moreover, candidate genes related to gender development were identified, shedding new insight on studying the mechanism of sex determination and differentiation in plant.

Citing Articles

Gene Regulatory Network Controlling Flower Development in Spinach ( L.).

Ma Y, Fu W, Wan S, Li Y, Mao H, Khalid E Int J Mol Sci. 2024; 25(11).

PMID: 38892313 PMC: 11173220. DOI: 10.3390/ijms25116127.

Spinach genomes reveal migration history and candidate genes for important crop traits.

Nguyen-Hoang A, Sandell F, Himmelbauer H, Dohm J NAR Genom Bioinform. 2024; 6(2):lqae034.

PMID: 38633427 PMC: 11023180. DOI: 10.1093/nargab/lqae034.

Comparative transcriptome analysis of dioecious floral development in Trachycarpus fortunei using Illumina and PacBio SMRT sequencing.

Xiao F, Zhao Y, Wang X, Mao Y, Jian X BMC Plant Biol. 2023; 23(1):536.

PMID: 37919651 PMC: 10623883. DOI: 10.1186/s12870-023-04551-x.

Highly sex specific gene expression in Jojoba.

Alsubaie B, Kharabian-Masouleh A, Furtado A, Al-Dossary O, Al-Mssallem I, Henry R BMC Plant Biol. 2023; 23(1):440.

PMID: 37726703 PMC: 10507870. DOI: 10.1186/s12870-023-04444-z.

Identifying Genes Associated with Female Flower Development of Rupr. Using a Transcriptomics Approach.

He L, Fan Y, Zhang Z, Wei X, Yu J Genes (Basel). 2023; 14(3).

PMID: 36980934 PMC: 10048520. DOI: 10.3390/genes14030661.

References

Lu P, Chai M, Yang J, Ning G, Wang G, Ma H . The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis. Plant Physiol. 2014; 164(4):1893-904. PMC: 3982751. DOI: 10.1104/pp.113.233387. View

Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley D . Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012; 7(3):562-78. PMC: 3334321. DOI: 10.1038/nprot.2012.016. View

Seifert G, Barber C, Wells B, Roberts K . Growth regulators and the control of nucleotide sugar flux. Plant Cell. 2004; 16(3):723-30. PMC: 385283. DOI: 10.1105/tpc.019661. View

Mandadi K, Scholthof K . Genome-wide analysis of alternative splicing landscapes modulated during plant-virus interactions in Brachypodium distachyon. Plant Cell. 2015; 27(1):71-85. PMC: 4330581. DOI: 10.1105/tpc.114.133991. View

Tang L, Chu H, Yip W, Yeung E, Lo C . An anther-specific dihydroflavonol 4-reductase-like gene (DRL1) is essential for male fertility in Arabidopsis. New Phytol. 2008; 181(3):576-87. DOI: 10.1111/j.1469-8137.2008.02692.x. View

Li Y, Van den Ende W, Rolland F . Sucrose induction of anthocyanin biosynthesis is mediated by DELLA. Mol Plant. 2013; 7(3):570-2. DOI: 10.1093/mp/sst161. View

Yu L, Ma X, Deng B, Yue J, Ming R . Construction of high-density genetic maps defined sex determination region of the Y chromosome in spinach. Mol Genet Genomics. 2020; 296(1):41-53. DOI: 10.1007/s00438-020-01723-4. View

Renner S . The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot. 2014; 101(10):1588-96. DOI: 10.3732/ajb.1400196. View

Quesada V, Macknight R, Dean C, Simpson G . Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO J. 2003; 22(12):3142-52. PMC: 162157. DOI: 10.1093/emboj/cdg305. View

10.

Mori K, Shirasawa K, Nogata H, Hirata C, Tashiro K, Habu T . Identification of RAN1 orthologue associated with sex determination through whole genome sequencing analysis in fig (Ficus carica L.). Sci Rep. 2017; 7:41124. PMC: 5264649. DOI: 10.1038/srep41124. View

11.

Sobral R, Silva H, Morais-Cecilio L, Costa M . The Quest for Molecular Regulation Underlying Unisexual Flower Development. Front Plant Sci. 2016; 7:160. PMC: 4759290. DOI: 10.3389/fpls.2016.00160. View

12.

Pfent C, Pobursky K, Sather D, Golenberg E . Characterization of SpAPETALA3 and SpPISTILLATA, B class floral identity genes in Spinacia oleracea, and their relationship to sexual dimorphism. Dev Genes Evol. 2005; 215(3):132-42. DOI: 10.1007/s00427-004-0459-4. View

13.

Song S, Qi T, Huang H, Xie D . Regulation of stamen development by coordinated actions of jasmonate, auxin, and gibberellin in Arabidopsis. Mol Plant. 2013; 6(4):1065-73. DOI: 10.1093/mp/sst054. View

14.

Picq S, Santoni S, Lacombe T, Latreille M, Weber A, Ardisson M . A small XY chromosomal region explains sex determination in wild dioecious V. vinifera and the reversal to hermaphroditism in domesticated grapevines. BMC Plant Biol. 2014; 14:229. PMC: 4167142. DOI: 10.1186/s12870-014-0229-z. View

15.

Li Q, Wang C, Jiang L, Li S, Sun S, He J . An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal. 2012; 5(244):ra72. DOI: 10.1126/scisignal.2002908. View

16.

Wang Z, Ji H, Yuan B, Wang S, Su C, Yao B . ABA signalling is fine-tuned by antagonistic HAB1 variants. Nat Commun. 2015; 6:8138. DOI: 10.1038/ncomms9138. View

17.

Kudoh T, Takahashi M, Osabe T, Toyoda A, Hirakawa H, Suzuki Y . Molecular insights into the non-recombining nature of the spinach male-determining region. Mol Genet Genomics. 2017; 293(2):557-568. DOI: 10.1007/s00438-017-1405-2. View

18.

Akagi T, Shirasawa K, Nagasaki H, Hirakawa H, Tao R, Comai L . The persimmon genome reveals clues to the evolution of a lineage-specific sex determination system in plants. PLoS Genet. 2020; 16(2):e1008566. PMC: 7048303. DOI: 10.1371/journal.pgen.1008566. View

19.

Tennessen J, Wei N, Straub S, Govindarajulu R, Liston A, Ashman T . Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries. PLoS Biol. 2018; 16(8):e2006062. PMC: 6128632. DOI: 10.1371/journal.pbio.2006062. View

20.

OMaoileidigh D, Wuest S, Rae L, Raganelli A, Ryan P, Kwasniewska K . Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell. 2013; 25(7):2482-503. PMC: 3753378. DOI: 10.1105/tpc.113.113209. View