Skip to main content
Log in

Rice Male Gamete Expression Database (RMEDB): A Web Resource for Functional Genomic Studies of Rice Male Organ Development

  • Technical Report
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Oryza sativa (rice) is an economically important crop, which is valued as a staple food source and as genetic model for cereals. Rice production needs to increase substantially to meet the growing global demand. Genetic studies have indicated that anther and pollen development genes can be used as targets to improve yield. Although several genes related to male organ developmental pathways have been characterized, the complete signaling network remains unclear. We used publicly available anther and pollen development transcriptome datasets to identify candidates for functional genomics studies. In addition, we newly generated RNA-Seq data for anther, anther wall and pollen samples with leaf sheath as control to provide the expression data for genes that are not covered by microarray technologies in rice. We constructed a platform, the rice male gamete expression database (RMEDB), comprising microarray and RNA-Seq based 188 transcriptome samples across diverse rice tissues and developmental stages of O. sativa japonica and O. sativa indica. Meta-expression analysis identified genes expressed at specific stages of anther or pollen developments. The functionalities in RMEDB database (http://ricephylogenomics-khu.org/RMEDB/home.php) can serve to identify candidates in male organ development for functional genomic studies of rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data Availability

All newly generated RNASeq raw reads are deposited in ArrayExpress. Mature anther, anther wall and pollen samples are provided under accession number E-MTAB-7974. Leaf sheath data is deposited under accession number E-MTAB-8353.

References

  • Aya K, Suzuki G, Suwabe K, Hobo T, Takahashi H, Shiono K, Yano K, Tsutsumi N, Nakazono M, Nagamura Y, Matsuoka M, Watanabe M (2011) Comprehensive network analysis of anther-expressed genes in rice by the combination of 33 laser microdissection and 143 spatiotemporal microarrays. PLoS ONE 6:e26162

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, Kakei Y, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK (2009) OsYSL18 is a rice iron(III)–deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol 70(6):68–692

    Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao P, Jung KH, Choi D, Hwang D, Zhu J, Ronald PC (2012) The rice Oligonucleotide array database: an atlas of rice gene expression. Rice 5:17

    PubMed  PubMed Central  Google Scholar 

  • Chhun T, Aya K, Asano K, Yamamoto E, Morinaka Y, Watanabe M, Kitano H, Ashikari M, Matsuoka M, Ueguchi-Tanaka M (2007) Gibberellin regulates pollen viability and pollen tube growth in rice. Plant Cell 19:3876–3888

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cui R, Han J, Zhao S, Su K, Wu F, Du X, Xu Q, Chong K, Theißen G, Meng Z (2010) Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). Plant J 61(5):767–781

    CAS  PubMed  Google Scholar 

  • Cui X, Lv Y, Chen M, Nikoloski Z, Twell D, Zhang D (2015) Young genes out of the male: an insight from evolutionary age analysis of the pollen transcriptome. Mol Plant 8:935–945

    CAS  PubMed  Google Scholar 

  • Duan Y, Xing Z, Diao Z, Xu W, Li S, Du X, Wu G, Wang C, Lan T, Meng Z (2012) Characterization of Osmads6-5, a null allele, reveals that OsMADS6 is a critical regulator for early flower development in rice (Oryza sativa L.). Plant Mol Biol 80(4–5):429–442

    CAS  PubMed  Google Scholar 

  • Fujii S, Yamada M, Toriyama K (2009) Cytoplasmic male sterility-related protein kinase, OsNek3, is regulated downstream of mitochondrial protein phosphatase 2C, DCW11. Plant Cell Physiol 50:828–837

    CAS  PubMed  Google Scholar 

  • Gao X, Liang W, Yin C, Ji S, Wang H, Su X, Guo C, Kong H, Xue H, Zhang D (2010) The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development. Plant Physiol 153(2):728–740

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57:876–891

    PubMed  PubMed Central  Google Scholar 

  • Gong P, He C (2014) Uncovering divergence of rice exon junction complex core heterodimer gene duplication reveals their essential role in growth, development, and reproduction. Plant Physiol 165:1047–1061

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta V, Khurana R, Tyagi AK (2007) Promoters of two anther-specific genes confer organ-specific gene expression in a stage-specific manner in transgenic systems. Plant cell Rep 26:1919–1931

    CAS  PubMed  Google Scholar 

  • Han MJ, Jung KH, Yi G, An G (2011) Rice importin β1 gene affects pollen tube elongation. Mol Cells 31:525–530

    Google Scholar 

  • Huang J, Zhao X, Cheng K, Jiang Y, Ouyang Y, Xu C, Li X, Xiao J, Zhang Q (2013) OsAP65, a rice aspartic protease, is essential for male fertility and plays a role in pollen germination and pollen tube growth. J Exp Bot 64:3351–3360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang SY, Cai M, Ramachandran S (2005) The Oryza sativa no pollen (Osnop) gene plays a role in male gametophyte development and most likely encodesa C2-GRAM domain-containing protein. Plant Mol Biol 57(6):835–853

    CAS  PubMed  Google Scholar 

  • Jung K, Han M, Lee Y, Kim Y, Hwang I, Kim M, Kim Y, Nahm BH, An G (2005) Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17(10):2705-2722

  • Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 Is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18:3015–3032

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kanneganti V, Gupta AK (2009) Isolation and Expression analysis of OsPME1, encoding for a putative Pectin Methyl Esterase from Oryza sativa (subsp.indica). Physiol Mol Biol Plants 15(2):123–131

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim E, Kim Y, Hong W, Lee C, Jeon JS, Jung KH (2019) Genome-wide analysis of root hair preferred RBOH genes suggests that three RBOH genes are associated with auxin-mediated root hair development in rice. J Plant Biol 62:229–238

    CAS  Google Scholar 

  • Ko S, Li M, Ku MS, Ho Y, Lin Y, Chuang M, Hsing H, Lien Y, Yang H, Chang H (2014) The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26(6):2486–2504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kurusu T, Koyano T, Hanamata S, Kubo T, Noguchi Y, Yagi C, Nagata N, Yamamoto T, Ohnishi T, Okazaki Y, Kitahata N, Ando D, Ishikawa M, Wada S, Miyao A, Hirochika H, Shimada H, Makino A, Saito K, Ishida H, Kinoshita T, Kurata N, Kuchitsu K (2014) OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. Autophagy 10:878–888

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Liang W, Hu Y, Zhu L, Yin C, Xu J, Dreni L, Kater MM, Zhang D (2011) Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13, and DROOPING LEAF in specifying floral organ identities and meristem fate. Plant Cell 23(7):2536–2552

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y (2010) Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22(1):173–190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Cui S, Wu F, Yan S, Lin X, Du X, Chong K, Schilling S, Theißen G, Meng Z (2013) Functional conservation of MIKC*-Type MADS box genes in Arabidopsis and rice pollen maturation. Plant Cell 25(4):1288–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Li W, Huang B, Cao X, Zhou X, Ye S, Li C, Gao F, Zou T, Xie K, Ren Y, Ai P, Tang Y, Li X, Deng Q, Wang S, Zheng A, Zhu J, Liu H, Wang L, Li P (2013) Natural variation in PTB1 regulates rice seed setting rate by controlling pollen tube growth. Nat Commun 4:1–13

    Google Scholar 

  • Li Y, Xiao J, Chen L, Huang X, Cheng Z, Han B, Zhang Q, Wu C (2018) Rice functional genomics research: past decade and future. Mol Plant 11:359–380

    CAS  PubMed  Google Scholar 

  • Liao Y, Smyth GK, Shi W (2014) FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930

    CAS  PubMed  Google Scholar 

  • Liu L, Zheng C, Kuang B, Wei L, Yan L, Wang T (2016) Receptor-like kinase RUPO interacts with potassium transporters to regulate pollen tube growth and integrity in rice. PLoS Genet 12:e1006085

    PubMed  PubMed Central  Google Scholar 

  • Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, Zhang Q, Guo J, Zhuang C, Mei M, Xia J, Wang L, Wu H, Liu YG (2008) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci USA 105:1–6

    Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:1–21

    Google Scholar 

  • Moon S, Oo MM, Kim B, Koh H, Oh SA, Yi G, An G, Park SK, Jung K (2018) Genome-wide analyses of late pollen-preferred genes conserved in various rice cultivars and functional identification of a gene involved in the key processes of late pollen development. Rice 11(1):28

    PubMed  PubMed Central  Google Scholar 

  • Moon S, Kumar A, Chandran N, Kim Y, Gho Y, Hong WJ, An G, Lee C, Jung KH (2019) Rice RHC encoding a putative cellulase is essential for normal root hair elongation. J Plant Biol 62:82–91

    CAS  Google Scholar 

  • Nakazono M, Qiu F, Borsuk LA, Schnable PS (2003) Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types : identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15:583–596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ngampanya B, Sobolewska A, Takeda T, Toyofuku K, Narangajavana J, Ikeda A, Yamaguchi J (2003) Characterization of rice functional monosaccharide transporter, OsMST5. Biosci Biotechnol Biochem 67(3):55–562

    Google Scholar 

  • Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47–e47

    PubMed  PubMed Central  Google Scholar 

  • Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134(4):1642–1653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Antonio BA, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res 39:1141–1148

    Google Scholar 

  • Shi J, Cui M, Yang L, Kim YJ, Zhang D (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci 20:741–753

    CAS  PubMed  Google Scholar 

  • Tanaka N, Uraguchi S, Saito A, Kajikawa M, Kasai K, Sato Y, Nagamura Y, Fujiwara T (2013) Roles of pollen-specific boron efflux transporter, OsBOR4, in the rice fertilization process. Plant Cell Physiol 54:2011–2019

    CAS  PubMed  Google Scholar 

  • Wilson ZA, Zhang DB (2009) From arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492

    CAS  PubMed  Google Scholar 

  • Xie Y, Niu B, Long Y, Li G, Tang J, Zhang Y, Ren D, Liu YG, Chen L (2017) Suppression or knockout of SaF/SaM overcomes the Sa-mediated hybrid male sterility in rice. J Integr Plant Biol 59:669–679

    CAS  PubMed  Google Scholar 

  • Yao W, Li G, Yu Y, Ouyang Y (2018) funRiceGenes dataset for comprehensive understanding and application of rice functional genes. Gigascience 7:1–9

    PubMed  Google Scholar 

  • Yi J, An S, An G (2014) OsMLO12, encoding seven transmembrane proteins, is involved with pollen hydration in rice. Plant reprod 27(4):169–180

    CAS  PubMed  Google Scholar 

  • Zhang D, Liang W, Yuan Z, Li N, Shi J, Wang J, Liu Y, Yu W, Zhang D (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Molecular Plant 1(4):599–610

    CAS  PubMed  Google Scholar 

  • Zhang K, Song Q, Wei Q, Wang C, Zhang L, Xu W, Su Z (2016) Down-regulation of OsSPX1 caused semi-male sterility, resulting in reduction of grain yield in rice. Plant Biotechnol J 14:1661–1672

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Z, Zhang Y, Liu X, Zhang X, Liu S, Yu X, Ren Y, Zheng X, Zhou K, Jiang L, Guo X, Gai Y, Wu C, Zhai H, Wang H, Wan J (2013) A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev Cell 27:113–122

    CAS  PubMed  Google Scholar 

  • Zhu QH, Ramm K, Shivakkumar R, Dennis ES, Upadhyaya NM (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiol 135:1514–1525

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu L, Shi J, Zhao G, Zhang D, Liang W (2013) Post-meiotic deficient anther1 (PDA1) encodes an ABC transporter required for the development of anther cuticle and pollen exine in rice. J Plant Biol 56:59–68

    CAS  Google Scholar 

  • Zhang Q, Li Z, Yang J, Li S, Yang D, Zhu Y (2012) A calmodulin-binding protein from rice is essential to pollen development. J Plant Biol 55(1):8–14

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Next-Generation BioGreen 21 Program (PJ01366401 to KHJ and PJ01369001 to SKP), the Rural Development Administration, Republic of Korea.

Author information

Authors and Affiliations

Authors

Contributions

AKNC, SKP, and KHJ designed the research. AKNC, AB, WJH, JWL and YJK performed the experiments and analyzed the data. AKNC, SKP, and KHJ wrote the manuscript.

Corresponding authors

Correspondence to Soon Ki Park or Ki-Hong Jung.

Ethics declarations

Conflict of interest

The author(s) declare no competing interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chandran, A.K.N., Hong, WJ., Abhijith, B. et al. Rice Male Gamete Expression Database (RMEDB): A Web Resource for Functional Genomic Studies of Rice Male Organ Development. J. Plant Biol. 63, 421–430 (2020). https://doi.org/10.1007/s12374-020-09267-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-020-09267-1

Keywords

Navigation