Skip to main content
Log in

Differential expression of transport and signalling genes in leaves and panicle regulates the development of pollen-free anthers in TGMS red rice

  • Original Paper
  • Published:
Cereal Research Communications Aims and scope Submit manuscript

Abstract

Thermosensitive genic male sterile (TGMS) plants are male sterile above a critical sterility temperature (CST) and become male fertile below CST during a critical thermosensitive stage. It is essential to analyse the gene expression pattern under fertility- and sterility-inducing conditions to understand the mechanisms of male sterility since it is regulated by a single recessive nuclear gene sensitive to environment during a specific stage of panicle development. Hence, this study aims at understanding the molecular mechanism associated with pollen sterility in TGMS system. The newly developed TGMS line on red rice background exhibited male sterility with pollen-free anthers and hence can be recommended as a stable female parent for the development of suitable red rice hybrids to the state of Kerala. Microarray gene expression analysis of TGMS leaf and young panicle revealed that occurrence of pollen-free anthers in the TGMS line during sterility-inducing condition is mainly due to the down-regulation of genes encoding ABC transporter proteins, lipid transfer protein and strictosidine synthase, glucose-methanol-choline oxidoreductase, male sterility protein 2, wax synthase and β-1,3-glucanase. Moreover, pathways involved in the carbohydrate synthesis and transport were also down-regulated during sterility condition. The differential expression of transport and signalling genes regulates the development of pollen-free anthers in TGMS 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.

Similar content being viewed by others

Availability of data and material

The experimental material was developed by the second author through funding from Kerala Biotechnology commission.

References

  • Ali J, Siddiq EA, Zaman FU, Abraham MJ, Ahamed IM (1995) Identification and characterization of temperature sensitive genic male sterile sources in rice. Indian J Genetics 55(3):243–259

    Google Scholar 

  • Biancucci M, Mattioli R, Forlani G, Funck D, Costantino P, Trovato M (2015) Role of proline and GABA in sexual reproduction of angiosperms Frontiers. Plant Sci 6:680

    Google Scholar 

  • Borkakati RR, Virmani SS (1996) Genetics of thermosensitive genic male sterility in rice. Euphytica 88:1–7

    Article  Google Scholar 

  • Borkakati RP, Virmani SS (1997) Determination of critical stage of fertility alteration in two thermosensitive genic male sterile mutants of rice In: Proc. Int. Symp. on Two-Line System of Heterosis Breeding in Crops Sep. 6–8, 1997, China National Hybrid Rice Research and Development Center, Changsha, China, pp 188–192

  • Celine NVJ, Roy S, Manju RV, Shabana R (2014) Phenological, morpho-agronomic and floral characterization of promising thermo sensitive genic male sterile rice (Oryza sativa L) lines suitable for Kerala. J Plant Sci Res 30(2):133–139

    Google Scholar 

  • Chang Z, Jin M, Yan W, Chen H, Qiu S, Fu S, Xia J, Liu Y, Chen Z, Wu J, Tang X (2018) The ATP-binding cassette (ABC) transporter OsABCG3 is essential for pollen development in rice. Rice 11:58

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19:847–861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Xu J, Devis D, Shi J, Ren K, Searle I, Zhang D (2016) Origin and functional prediction of pollen allergens in plants. Plant Physiol 172:341–357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chueasiri C, Chunthong K, Pitnjam K, Chakhonkaen S, Sangarwut N, Sangsawang K, Suksangpanomrung M, Michaelson LV, Napier JA, Muangprom A (2014) Rice ORMDL controls sphingolipid homeostasis affecting fertility resulting from abnormal pollen development. PLoS ONE 9(9):1–14

    Article  CAS  Google Scholar 

  • Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42:315–328

    Article  CAS  PubMed  Google Scholar 

  • Fu Z, Yu J, Cheng X, Zong X, Xu J, Chen M, Li Z, Zhang D, Liang W (2014) The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 26:1512–1524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Funck D, Winter G, Baumgarten L, Forlani G (2012) Requirement of proline synthesis during Arabidopsis reproductive development. BMC Plant Biol 12:191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groot P, Weterings K, Been M, Wittink F, Hulzink R, Custers J, Herpen M, Wullems G (2004) Silencing of the pollen-specific gene NTP303 and its family members in tobacco affects in vivo pollen tube growth and results in male sterile plants. Plant Mol Biol 55:715–726

    Article  PubMed  Google Scholar 

  • Hafidh S, Potesil D, Muller K, Fila J, Michailidis C, Herrmannova A, Fecikova J, Ischebeck T, Valasek LS, Zdrahal Z, Honysa D (2018) Dynamics of the pollen sequestrome defined by subcellular coupled omics. Plant Physiol 178:258–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments a review. Plant Signal Behav 7(11):1456–1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Hoque MA, Burritt DJ, Fujita M (2014) Proline protects plants against abiotic oxidative stress: biochemical and molecular mechanisms. In: Ahmad P (ed.) Oxidative Damage to Plants Antioxidant Networks and Signaling Academic Press, United States of America, pp 477–522

  • Huang M, Chen TL, Huang AHC (2013) Abundant Type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiol 163:1218–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Zhi-Guo E, Zhang H, Shu Q (2014) Workable male sterility systems for hybrid rice: Genetics, biochemistry, molecular biology and utilization. Rice 7(13):1–14

    Google Scholar 

  • Ji C, Li H, Chen L, Xie M, Wang F, Chen Y, Liu YG (2013) A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development. Mol Plant 6:1715–1718

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung K, Han M, Lee D, Lee Y, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim Y, Hwang I, Gr A (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung J, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JCW, Schafer E, Jaeger KE, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354(6314):886–889

    Article  CAS  PubMed  Google Scholar 

  • Kater MM, Dreni L, Colombo L (2006) Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J Exp Bot 57(13):3433–3444

    Article  CAS  PubMed  Google Scholar 

  • Ko SS, Li MJ, Ku MS, Ho YC, Lin YJ, Chuang MH, Hsing HX, Lien YC, Yang HT, Chang HC, Chan MT (2014) The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26:2486–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ku S, Yoon H, Suh HS, Chung Y (2003) Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217:559–565

    Article  CAS  PubMed  Google Scholar 

  • Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice mads box genes with similarity to Arabidopsis Class A. B and C genes Plant Cell Physiol 41(6):710–718

    Article  CAS  Google Scholar 

  • Lai C, Kunst L, Jetter R (2007) Composition of alkyl esters in the cuticular wax on inflorescence stems of Arabidopsis thaliana cer mutants. Plant J 50:189–196

    Article  CAS  PubMed  Google Scholar 

  • Li H, Zhang D (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5(9):1121–1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Zhang D, Liu H, Yin C, Li X, Liang W, Yuan Z, Xu B, Chu H, Wang J, Wen T, Huang H, Luo D, Ma H, Zhang D (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Liang W, Hu Y, Zhu L, Yin C, Xu J, Dreni L, Kater MM, Zhang D (2011a) 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 23:2536–2552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011b) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Li D, Guo Z, Shi Q, Xiong S, Zhang C, Zhu J, Yang Z (2016) OsACOS12, an orthologue of Arabidopsis acyl-CoA synthetase5, plays an important role in pollen exine formation and anther development in rice. BMC Plant Biol 16:256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin M, Chai K, Ko S, Kuang L, Lur H, Charng Y (2014) A positive feedback loop between heat shock protein101 and heat stress-associated 32-kDa protein modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol 164:2045–2053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin H, Yu J, Pearce P, Zhang D, Wilson ZA (2017) RiceAntherNet: a gene co-expression network for identifying anther and pollen development genes. Plant J 92(6):1076–1091

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Gu F, Dong S, Liu W, Wang H, Chen Z, Wang J (2016) CONSTANS-like 9 (COL9) delays the flowering time in Oryza sativa by repressing the Ehd1 pathway. Biochem Biophys Res Commun 479:173e178

    Article  Google Scholar 

  • Liu Z, Lin S, Shi J, Yu J, Zhu L, Yang X, Zhang D, Liang W (2017) Rice No Pollen 1 (NP1) is required for anther cuticle formation and pollen exine patterning. Plant J 91(2):263–277

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Zhang G, Wang J, Li J, Song Y, Qiao L, Niu N, Wang J, Ma S, Li L (2018) Chemical hybridizing agent SQ-1-induced male sterility in Triticum aestivum L a comparative analysis of the anther proteome. BMC Plant Biol 18:7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mattioli R, Biancucci M, Shall AE, Mosca L, Costantino P, Funck D, Trovato M (2018) Proline synthesis in developing microspores is required for pollen development and fertility. BMC Plant Biol 18:356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ni E, Zhou L, Li J, Jiang D, Wang Z, Zheng S, Qi H, Zhou Y, Wang C, Xiao S, Liu Z, Zhou H, Zhuang C (2018) OsCER1 plays a pivotal role in very-long-chain alkane biosynthesis and affects plastid development and programmed cell death of tapetum in rice (Oryza sativa L). Front Plant Sci 9:1217

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan Y, Li Q, Wang Z, Wang Y, Ma R, Zhu L, He G, Chen R (2014) Genes associated with thermosensitive genic male sterility in rice identified by comparative expression profiling. BMC Genom 15:1114

    Article  CAS  Google Scholar 

  • Pearce S, Ferguson A, King J, Wilson Z (2015) FlowerNet: a gene expression correlation network for anther and pollen development. Plant Physiol 167:1717–1730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranjan R, Khurana R, Malik N, Badoni S, Parida SK, Kapoor S, Tyagi AK (2017) bHLH142 regulates various metabolic pathway-related genes to affect pollen development and anther dehiscence in rice. Sci Rep 7:43397

    Article  PubMed  PubMed Central  Google Scholar 

  • Reddy OUK, Siddiq EA, Sarma NP, Ali J, Hussain AJ, Nimmakayala P, Ramasamy P, Pammi S, Reddy AS (2000) Genetic analysis of temperature-sensitive male sterility in rice. Theor Appl Genet 100:794–801

    Article  CAS  Google Scholar 

  • Rekha KS, Kumar M, Saraswathi R, Mannonmani S, Raveendran M (2017) Study on critical stages and critical sterility point of thermo-sensitive genic male sterile lines of rice for two line hybrid production. Int J Curr Microbiol App Sci 6(5):2128–2135

    Article  Google Scholar 

  • Rieu I, Twell D, Firon N (2017) Pollen development at high temperature: from acclimation to collapse. Plant Physiol 173:1967–1976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salminen TA, Blomqvist K, Edqvist J (2016) Lipid transfer proteins: classification, nomenclature, structure and function. Planta 244:971–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu Y, Lee PY, Truong M, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Scarpin MR, Sigaut L, Temprana SG, Boccaccio GL, Pietrasanta LI, Muschietti JP (2017) Two Arabidopsis late pollen transcripts are detected in cytoplasmic granules. Plant direct 1(4):e00012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shi X, Han X, Lu T (2016) Callose synthesis during reproductive development in monocotyledonous and dicotyledonous plants. Plant Signal Behav 11(2):e1062196

    Article  PubMed  CAS  Google Scholar 

  • Shuai B, Reynaga-Pen CG, Springer PS (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song J, Liu Q, Hu B, Wu W (2017) Photoreceptor PhyB involved in Arabidopsis temperature perception and heat-tolerance formation. Int J Mol Sci 18:1194–11107

    Article  PubMed Central  CAS  Google Scholar 

  • Souza CA, Kim SS, Koch S, Kienow L, Schneider K, McKim SM, Haughn GW, Kombrink E, Douglas CJ (2009) Novel Fatty Acyl-CoA Synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell 21:507–525

    Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2010) Plant Physiology (5th Ed) Sinauer Associates Inc. Publishers, Massachusetts, USA, 778p

  • Taoka K, Ohki K, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri YA, Tamaki S, Ogaki Y, Nakagawa SC, Kojima C, Shimamoto K (2011) 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476:332–337

    Article  CAS  PubMed  Google Scholar 

  • Tian HQ, Kuang A, Musgrave ME, Russel SD (1998) Calcium distribution in fertile and sterile anthers of a photoperiod-sensitive genic male-sterile rice. Planta 204:183–192

    Article  CAS  Google Scholar 

  • Virmani SS, Viraktamath BC, Casal CL, Toledo RS, Lopez MT, Manalo JO (1997) Hybrid Rice Breeding Manual. International Rice Research Institute, Los Banos, p 194p

    Google Scholar 

  • Wan L, Zha W, Cheng X, Liu C, Lv L, Liu C, Wang Z, Du B, Chen R, Zhu L, He G (2011) A rice-1,3-glucanase gene Osg1 is required for callose degradation in pollen development. Planta 233:309–323

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Tian Q, Zhou S, Mao D, Chen L (2019) A quantitative proteomic analysis of the molecular mechanism underlying fertility conversion in thermo-sensitive genetic male sterility line AnnongS-1 BMC. Plant Biol 19(1):65

    Google Scholar 

  • Wu W, Zheng X, Chena D, Zhang Y, Mab W, Zhang H, Suna L, Yanga Z, Zhao C, Zhana X, Shena X, Yu P, Fu Y, Zhu S, Cao L, Cheng S (2017) OsCOL16, encoding a CONSTANS-like protein, represses flowering by up-regulating Ghd7 expression in rice. Plant Sci 260:1–25

    Article  PubMed  CAS  Google Scholar 

  • Xiao X, Yang Y, Yang Y, Lin J, Tang D, Liu X (2009) Comparative analysis of young panicle proteomein thermo-sensitive genic male-sterile rice Zhu-1S under sterile and fertile conditions. Biotechnol Lett 31:157–161

    Article  CAS  PubMed  Google Scholar 

  • Xiao C, Somerville C, Andersona CT (2014) POLYGALACTURONASE INVOLVED IN EXPANSION1 functions in cell elongation and flower development in Arabidopsis. Plant Cell 26:1018–1035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D, Shi J, Rautengarten C, Yang L, Qian X, Uzair M, Zhu L, Luo Q, An G, Wabmann F, Schreiber L, Heazlewood JL, Hu SH, Zhang J, Liang W (2017a) Defective Pollen Wall 2 (DPW2) encodes an acyl transferase required for rice pollen development. Plant Physiol 173:240–255

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Liu S, Liu Y, Ling S, Chen C, Yao J (2017b) HOTHEAD-Like HTH1 is involved in anther cutin biosynthesis and is required for pollen fertility in rice. Plant Cell Physiol 58(7):1238–1248

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Lai Y, Li M, Xu W, Xue Y (2008) A Novel C2-domain phospholipid-binding protein, OsPBP1, is required for pollen fertility in rice. Mol Plant 1(5):770–785

    Article  CAS  PubMed  Google Scholar 

  • Yang K, Xia C, Liu X, Dou X, Wang W, Chen L, Zhang X, Xie L, He L, Ma X, Ye D (2009) A mutation in THERMOSENSITIVE MALE STERILE 1, encoding a heat shock protein with DnaJ and PDI domains, leads to thermosensitive gametophytic male sterility in Arabidopsis. Plant J 57:870–882

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Wu D, Shi J, He Y, Pinot F, Grausem B, Yin C, Zhu L, Chen M, Luo Z, Liang W, Zhang D (2014) Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine. J Integr Plant Biol 56(10):979–994

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Ma Y, Li J (2016) The rice YABBY4 gene regulates plant growth and development through modulating the gibberellin pathway. J Exp Bot 67(18):5545–5556

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Liang W, Chen M, Zhang D, Zhao X, Shi J (2017) Rice fatty acyl-CoA synthetase OsACOS12 is required for tapetum programmed cell death and male fertility. Planta 246:1–18

    Article  CAS  Google Scholar 

  • Yu J, Meng Z, Liang W, Behera S, Kudla J, Tucker MR, Luo Z, Chen M, Xu D, Zhao G, Wang J, Zhang S, Kim Y, Zhang D (2016) A rice Ca2+ binding protein is required for tapetum function and pollen formation. Plant Physiol 172:1772–1786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54(14):2343–2353

    Article  Google Scholar 

  • Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154:149–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xu C, He Y, Zong J, Yang X, Si H, Sun Z, Hu J, Liang W, Zhang D (2013) Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. PNAS 110(1):76–81

    Article  PubMed  Google Scholar 

  • Zhou H, Liu Q, Li J, Jiang D, Zhou L, Wu P, Lu S, Li F, Zhu L, Liu Z, Chen L, Liu Y, Zhuang C (2012) Photoperiod and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res 22:649–660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Zhou M, Yang Y, Li J, Zhu L, Jiang D, Dong J, Liu Q, Gu L, Zhou L, Feng M, Qin P, Hu X, Song C, Shi J, Song X, Ni E, Wu X, Deng Q, Liu Z et al (2014) RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nature Commun 5:2041–2743

    Article  Google Scholar 

  • Zou T, Xiao Q, Li W, Luo T, Yuan G, He Z, Liu M, Li Q, Xu P, Zhu J, Liang Y, Deng Q, Wang S, Zhen A, Wang L, Li P, Li S (2017) OsLAP6/OsPKS1, an orthologue of Arabidopsis PKSA/LAP6, is critical for proper pollen exine formation. Rice 10:53

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank the Associate Director of Research, Regional Agricultural Research Station (RARS), Ambalavayal, for permitting seed multiplication in the high altitude research station. Kerala Biotechnology commission is acknowledged for providing research grant to the second author through whom the experimental material was developed. The authors also thank Genotypic Technology Pvt Ltd., Bengaluru, for microarray gene expression analysis.

Funding

Not applicable

Author information

Authors and Affiliations

Authors

Contributions

The first and the second author conceived and designed the research; the first author conducted the experiment, analysed the data and wrote the manuscript

Corresponding author

Correspondence to Roy Stephen.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest

Additional information

Communicated by J. Zimny.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 992 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gayathri, R., Stephen, R. Differential expression of transport and signalling genes in leaves and panicle regulates the development of pollen-free anthers in TGMS red rice. CEREAL RESEARCH COMMUNICATIONS 49, 465–473 (2021). https://doi.org/10.1007/s42976-020-00124-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42976-020-00124-y

Keywords

Navigation