Exploring differentially expressed genes associated with fertility instability of S-type cytoplasmic male-sterility in maize by RNA-seq
SU Ai-guo*, SONG Wei*, SHI Zi, ZHAO Yan-xin, XING Jin-feng, ZHANG Ru-yang, LI Chun-hui, LUO Mei-jie, WANG Ji-dong, ZHAO Jiu-ran
Maize Research Center, Beijing Academy of Agriculture and Forestry Sciences/Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Beijing 100097, P.R.China
Abstract The germplasm resources for the S-type male sterility is rich in maize and it is resistant to Bipolaris maydis race T and CI, but the commercial application of S-type cytoplasmic male sterility (CMS-S) in maize hybrid industry is greatly compromised because of its common fertility instability. Currently, the existence of multiple minor effect loci in specific nuclear genetic backgrounds was considered as the molecular mechanism for this phenomenon. In the present study, we evaluated the fertility segregation of the different populations with the fertility instable material FIL-H in two environments of Beijing and Hainan, China. Our results indicated that the fertility instability of FIL-H was regulated by multiple genes, and the expression of these genes was sensitive to environmental factors. Using RNA sequencing (RNA-seq) technology, transcriptomes of the sterile plants and partially fertile plants resulted from the backcross of FIL-H×Jing 724 in Hainan were analyzed and 2 108 genes with different expression were identified, including 1 951 up-regulated and 157 down-regulated genes. The cluster analysis indicated that these differentially expressed genes (DEGs) might play roles in many biological processes, such as the energy production and conversion, carbohydrate metabolism and signal transduction. In addition, the pathway of the starch and sucrose metabolism was emphatically investigated to reveal the DEGs during the process of starch biosynthesis between sterile and partially fertile plants, which were related to the key catalytic enzymes, such as ADP-G pyrophosphorylase, starch synthase and starch branching enzyme. The up-regulation of these genes in the partially fertile plant may promote the starch accumulation in its pollen. Our data provide the important theoretical basis for the further exploration of the molecular mechanism for the fertility instability in CMS-S maize.
This work is supported by the National Key Technologies R&D Program of China during the 12th Five-Year Plan period (2014BAD01B09), the Beijing Postdoctoral Research Foundation, China (2014ZZ-68), the Sci-Technology Innovation Project of Beijing Academy of Agriculture and Forestry Science (BAAFS), China (KJCX20140202), the Innovative Team Construction Project of BAAFS, China (JNKYT201603) and the Postdoctoral Scientific Fund of BAAFS, China (2014013).
SU Ai-guo*, SONG Wei*, SHI Zi, ZHAO Yan-xin, XING Jin-feng, ZHANG Ru-yang, LI Chun-hui, LUO Mei-jie, WANG Ji-dong, ZHAO Jiu-ran.
2017.
Exploring differentially expressed genes associated with fertility instability of S-type cytoplasmic male-sterility in maize by RNA-seq. Journal of Integrative Agriculture, 16(08): 1689-1699.
Alexa A, Rahnenfuhrer J. 2010. TopGO: Enrichment analysis for gene ontology. R package ver. 2.8.
Anders N, Juergens G. 2008. Large ARF guanine nucleotide exchange factors in membrane trafficking. Cellular and Molecular Life Sciences, 65, 3433–3445.
Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology, 11, 1–12.
Ashburner M. 2000. Gene Ontology: Tool for the unification of biology. Nature Genetics, 25, 25–29.
Baguma Y, Sun C, Ahlandsberg S, Mutisya J, Palmqvist S, Rubaihayo P R, Magambo M J, Egwang T G, Larsson H, Jansson C. 2003. Expression patterns of the gene encoding starch branching enzyme II in the storage roots of cassava (Manihot esculenta Crantz). Plant Science, 164, 833–839.
Ballicora M A, Iglesias A A, Preiss J. 2003. ADP-glucose pyrophosphorylase, a regulatory enzyme for bacterial glycogen synthesis. Microbiology & Molecular Biology Reviews, 67, 213–225.
Beckett J B. 1971. Classification of male-sterile cytoplasms in maize (Zea mays L.). Crop Science, 11, 724–727.
Bohra A, Jha U C, Adhimoolam P, Bisht D, Singh N P. 2016. Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Reports, 35, 967–993.
Buckmann H, Thiele K, Schiemann J, Husken A. 2014. Influence of air temperature on the stability of cytoplasmic male sterility (CMS) in maize (Zea mays L.). Journal of Agrobiotechnology Management & Economics, 2, 205–212.
Charles S, Levings I. 1993. Thoughts on cytoplasmic male sterility in cms-T maize. The Plant Cell, 5, 1285–1290.
Deng Y Y, Li J Q, Wu S, Zhu Y P, Chen Y W, He F C. 2006. Integrated nr database in protein annotation system and its localization. Computer Engineering, 32, 71–72.
Duvick D N. 1965. Cytoplasmic pollen sterility in corn. Advances in Genetics, 13, 1–56.
Feng Y, Zheng Q, Song H, Wang Y, Wang H, Jiang L J, Yan J B, Zheng Y L, Yue B. 2015. Multiple loci not only Rf3 involved in the restoration ability of pollen fertility, anther exsertion and pollen shedding to S type cytoplasmic male sterile in maize. Theoretical and Applied Genetics, 128, 2341–2350.
Gabay-Laughnan S, Kuzmin E V, Monroe J, Roark L, Newton K J. 2009. Characterization of a novel thermosensitive restorer of fertility for cytoplasmic male sterility in maize. Genetics, 182, 91–103.
Hanson M R, Bentolila S. 2004. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. The Plant Cell, 16S, S154–S169.
Kamps T L, Chase C D. 1997. RFLP mapping of the maize gametophytic restorer-of-fertility locus (rf3) and aberrant pollen transmission of the nonrestoring rf3 allele. Theoretical and Applied Genetics, 95, 525–531.
Kanehisa M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Research, 32, 277–280.
Kubo T, Newton K J. 2008. Angiosperm mitochondrial genomes and mutations. Mitochondrion, 8, 5–14.
Kuhlmann N, Wroblowski S, Knyphausen P, De B S, Brenig J, Zienert A Y, Meyer-Teschendorf K, Praefcke G J, Nolte H, Krüger M. 2015. Structural and mechanistic insights into the regulation of the fundamental Rho-regulator RhoGDIα by lysine acetylation. Journal of Biological Chemistry, 291, 5484–5499.
Laser K D, Lersten N R. 1972. Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. The Botanical Review, 38, 425–454.
Li X Q, Wan B H, Liu J L, Zheng Y L, Li J, Xu S Z. 2004. Cytological observation on microspore genesis of WBMs a new line of S-CMS maize. Scientia Agricultura Sinica, 30, 304–307. (in Chinese)
Liu K M, Su H, Cui Y. 1991. Reaction of different male sterile cytoplasm subgroups of the C group maize to infection of Biploasris maydis race. Maize Science, 24, 58–60. (in Chinese)
Matera J T, Monroe J, Smelser W, Gabay-Laughnan S, Newton K J. 2011. Unique changes in mitochondrial genomes associated with reversions of S-type cytoplasmic male sterility in maizemar. PLoS One, 6, e23405.
Newton K J, Stern D B, Gabay-Laughnan S. 2009. Mitochondria and chloroplasts. In: Bennetzen J L, Hake S, eds. Handbook of Maize. Hake Springer, New York. pp. 481–503.
Rolf A, Amos B, Wu C H, Barker W C, Brigitte B, Serenella F, Elisabeth G, Huang H Z, Rodrigo L, Michele M. 2004. UniProt: The universal protein knowledgebase. Nucleic Acids Research, 32, 115–119.
Satoh H, Nishi A, Yamashita K, Takemoto Y, Tanaka Y, Hosaka Y, Sakurai A, Fujita N, Nakamura Y. 2003. Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiology, 133, 1111–1121.
Schulze S K, Kanwar R, Goelzenleuchter M, Therneau T M, Beutler A S. 2012. SERE: Single-parameter quality control and sample comparison for RNA-seq. BMC Genomics, 13, 1–9.
Song W, Su A G, Xing J F, Wu J F, Zhao J R. 2016. Study on breeding of new S-type cytoplasmic male sterile material from maize inbred line Jing 724 with molecular marker assisted selection. Journal of Maize Sciences, 24, 33–36. (in Chinese)
Stark D M, Timmerman K P, Barry G F, Preiss J, Gm K. 1992. Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science, 258, 287–292.
Su A G, Song W, Xing J F, Zhao Y X, Zhang R Y, Li C H, Duan M X, Luo M J, Shi Z, Zhao J R. 2016. Identification of genes potentially associated with the fertility instability of S-type cytoplasmic male sterility in maize via bulked segregant RNA-seq. PLOS ONE, 11, e0163489.
Tatusov R L, Galperin M Y, Natale D A, Koonin E V. 2000. The COG database: A tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Research, 28, 33–36.
Thorbjornsen T, Villand PKleczkowski L A, Olsen O A. 1996. A single gene encodes two different transcripts for ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochemical Journal, 313, 149–154.
Tie S G, Xia J H, Qiu F Z, Zheng Y L. 2006. Genome-wide analysis of maize cytoplasmic male sterility-S based on QTL mapping. Plant Molecular Biology Reporter, 24, 71–80.
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28, 511–515.
Van?etovi? J, Vidakovi? M, Ignjatovi?-Mici? D, Nikoli? A, Markovi? K, An?elkovi? V. 2010. The structure of sterile cytoplasm types within a maize genebank collection. Russian Journal of Genetics, 46, 836–840.
Wang Z, Chen X, Wang J, Liu T, Yan L, Li Z, Wang G. 2007. Increasing maize seed weight by enhancing the cytoplasmic ADP-glucose pyrophosphorylase activity in transgenic maize plants. Plant Cell Tissue and Organ Culture, 88, 83–92.
Weider C, Stamp P, Christov N, Hüsken A, Foueillassar X, Camp K H, Munsch M. 2009. Stability of cytoplasmic male sterility in maize under different environmental conditions. Crop Science, 49, 77–84.
Wen L Y, Chase C D. 1999. Pleiotropic effects of a nuclear restorer-of-fertility locus on mitochondrial transcripts in male-fertile and S male-sterile maize. Current Genetics, 35, 521–526.
Xu X B, Liu Z X, Zhang D F, Liu Y, Song W B, Li J S, Dai J R. 2009. Isolation and analysis of rice Rf1-orthologus PPR genes co-segregating with rf3 in maize. Plant Molecular Biology Reporter, 27, 511–517.
Zabala G, Gabay-Laughnan S, Laughnan J R. 1997. The nuclear gene Rf3 affects the expression of the mitochondrial chimeric sequence R implicated in S-type male sterility in maize. Genetics, 147, 847–860.
Zhang Z X, Tang W T, Zhang F D, Zheng Y L. 2005. Fertility restoration mechanisms in S-type cytoplasmic male sterility of maize (Zea mays L.) revealed through expression differences identified by cDNA microarray and suppression subtractive hybridization. Plant Molecular Biology Reporter, 23, 17–38.
Zheng Y L, Liu J L. 1992. Relativity between mitochondria DNA and fertility instability of CMS-C in maize. Journal of Huazhong Agricultural University, 11, 120–126. (in Chinese)
