Skip to main content
SpringerLink
Log in

Role of ABA Signaling in Regulation of Stem Sugar Metabolism and Transport under Post- Flowering Drought Stress in Sweet Sorghum

Plant Molecular Biology Reporter volume 37, pages 303–313 (2019)Cite this article

Abstract

Sugar remobilization from vegetative to reproductive tissues is an important process that determines grain yield in crops. Sweet sorghum stems store sugar and introgression of Stay green1 (Stg 1) locus from the grain sorghum genotype B35 into the sweet sorghum genotype S35 was previously shown to bring about a 2-fold higher stem sugar accumulation in the near-isogenic line (NIL) S35SG06040. We hypothesized that remobilization of stem sugar augments grain yield on exposure to drought stress and that the phytohormone abscisic acid (ABA) has a role to play in this process. ABA levels were three times higher in the NIL as compared to those in S35 on drought stress exposure. Remobilization of stem sugars in the NIL was evident by the observed decrease in reducing sugar content in the stem but not in the peduncle in response to prolonged drought stress exposure. Drought-induced expression of some ABA response factors (ABFs) as well as invertase and sucrose transporter genes was seen to be higher in the NIL as compared to S35. An over-representation of ABA-responsive elements (ABREs) and sugar signaling motifs in the differentially expressed genes indicated the involvement of ABA and sugar signaling in regulation of their expression. Two ABF genes located on the Stg1 locus showed single nucleotide polymorphism, which possibly accounted for their differential regulation in S35 and the NIL. The results suggest that ABA signaling plays an important role in post-flowering drought-induced remobilization of sugars to the reproductive sinks.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (Canada)

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

References

  • Blum A (2005) Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive? Aust J Agri Res 56:1159–1168

    Article  Google Scholar 

  • Blum A, Golan G, Mayer J, Sinmena B (1997) The effect of dwarfing genes on sorghum grain. filling from remobilized stem reserves, under stress. Field Crop Res 52:43–54

    Article  Google Scholar 

  • Braun DM, Wang L, Ruan YL (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signaling to enhance crop yield and food security. J Exp Bot 65:1713–1735

    Article  CAS  Google Scholar 

  • Calviño M, Bruggmann R, Messing J (2011) Characterization of the small RNA component of the transcriptome from grain and sweet sorghum stems. BMC Genomics 12:356–367

    Article  Google Scholar 

  • Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element bindingfactors. J Biol Chem 275:1723–1730

    Article  CAS  Google Scholar 

  • Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488

    Article  CAS  Google Scholar 

  • Ghate T, Deshpande S, Bhargava S (2017) Accumulation of stem sugar and its remobilisation in response to drought stress in a sweet sorghum genotype and its near-isogenic lines carrying different stay-green loci. Plant Biol 19:396–405

    Article  CAS  Google Scholar 

  • Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signaling network. J Exp Bot 55:253–264

    Article  CAS  Google Scholar 

  • Guan Y, Ren H, Xie H, Ma Z, Chen F (2009) Identification and characterization of bZIP-type. transcription factors involved in carrot (Daucus carota L.) somatic embryogenesis. Plant J 60:207–217

    Article  CAS  Google Scholar 

  • Harris K, Subudhi PK, Borrell A, Jordan D, Rosenow D, Nguyen H, Klein P, Klein R, Mullet J (2006) Sorghum stay-green QTL individually reduce post-flowering drought-induced leaf senescence. J Exp Bot 58:327–338

    Article  Google Scholar 

  • Hwang YS, Karrer EE, Thomas BR, Chen L, Rodriguez RL (1998) Three cis-elements required for. rice α-amylase Amy3D expression during sugar starvation. Plant Mol Biol 36:331–341

    Article  CAS  Google Scholar 

  • Jaiswal V, Gahlaut V, Mathur S, Agarwal P, Khandelwal MK, Khurana JP et al (2015) Identification of novel SNP in promoter sequence of TaGW2-6A associated with grain weight and other agronomic traits in wheat (Triticum aestivum L.). PLoS One 10(6):e0129400

    Article  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  Google Scholar 

  • Johnson SM, Cummins I, Lim FL, Slabas AR, Knight MR (2015) Transcriptomic analysis. comparing stay-green and senescent Sorghum bicolor lines identifies a role for proline biosynthesis in the stay-green trait. J Exp Bot 66:7061–7073

    Article  CAS  Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  CAS  Google Scholar 

  • Lindlöf A, Bräutigam M, Chawade A, Olsson O, Olsson B (2009) In silico analysis of promoter. regions from cold-induced genes in rice (Oryza sativa L.) and Arabidopsis thaliana reveals the importance of combinatorial control. Bioinformatics 25:1345–1348

    Article  Google Scholar 

  • Ling J, Luo Z, Liu F, Mao Z, Yang Y, Xie B (2017) Genome-wide analysis of microRNA targeting impacted by SNPs in cucumber genome. BMC Genomics 18:275–287

    Article  Google Scholar 

  • Lingle SE, Dunlap JR (1987) Sucrose metabolism in netted muskmelon fruit during development. Plant Physiol 84:386–389

    Article  CAS  Google Scholar 

  • Liu S, Li M, Su L, Ge K, Li L, Li X, Liu X, Li L (2016) Negative feedback regulation of ABA biosynthesis in peanut (Arachis hypogea): a transcription factor complex inhibits AhNCED1 expression during water stress. Sci Rep 6:37943–37954

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time. quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Luo J, Zhou JJ, Zhang JZ (2018) Aux/IAA gene family in plants: molecular structure, regulation and function. Int J Mol Sci 19:259–276

    Article  Google Scholar 

  • Ma QJ, Sun MH, Lu J, Liu YJ, Hu DG, Hao YJ (2017) Transcription factor AREB2 is involved in. soluble sugar accumulation by activating sugar transporter and amylase genes. Plant Physiol 174:2348–2362

    Article  CAS  Google Scholar 

  • Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem Sci 20:506–510

    Article  CAS  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Mizuno H, Kasuga S, Kawahigashi H (2016) The sorghum SWEET gene family: stem sucrose. accumulation as revealed through transcriptome profiling. Biotechnol Biofuels 9:127–138

    Article  Google Scholar 

  • Morikami A, Matsunaga R, Tanaka Y, Suzuki S, Mano S, Nakamura K (2005) Two cis-acting. regulatory elements are involved in the sucrose-inducible expression of the sporamin gene promoter from sweet potato in transgenic tobacco. Mol Gen Genomics 272:690–699

    Article  CAS  Google Scholar 

  • Muller B, Pantin F, Genard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits. uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729

    Article  CAS  Google Scholar 

  • Nakurte I, Keisa A, Rostoks N (2012) Development and validation of a reversed-phase liquid. chromatography method for the simultaneous determination of indole-3-acetic acid, indole-3-pyruvic acid, and abscisic acid in barley (Hordeum vulgare L.). J Anal Methods Chem 2012:103575–103580

    Article  Google Scholar 

  • Pollock C, Farrar J, Tomos D, Gallagher J, Lu C, Koroleva O (2003) Balancing supply and. demand: the spatial regulation of carbon metabolism in grass and cereal leaves. J Exp Bot 54:489–494

    Article  CAS  Google Scholar 

  • Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29:426–434

    Article  CAS  Google Scholar 

  • Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67

    Article  CAS  Google Scholar 

  • Ruuska SA, Rebetzke GJ, van Herwaarden AF, Richards RA, Fettell NA, Tabe L, Jenkins CL (2006) Genotypic variation in water-soluble carbohydrate accumulation in wheat. Funct Plant Biol 33:799–809

    Article  CAS  Google Scholar 

  • Shen Q, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-Box and a novel cis-acting element. Plant Cell 7:295–307

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shukla S, Felderhoff TJ, Saballos A, Vermerrisa W (2017) The relationship between plant height. and sugar accumulation in the stems of sweet sorghum (Sorghum bicolor (L.) Moench). Field Crop Res 203:181–191

    Article  Google Scholar 

  • Slewinski TL (2012) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. J Exp Bot 63:4647–4670

    Article  CAS  Google Scholar 

  • Tatematsu K, Ward S, Leyser O, Kamiya Y, Nambara E (2005) Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol 138:757–766

    Article  CAS  Google Scholar 

  • Trouverie J, Thevenot C, Rocher JP, Sotta B, Prioul JL (2003) The role of abscisic acid in the response of a specific vacuolar invertase to water stress in the adult maize leaf. J Exp Bot 5:2177–2186

    Article  Google Scholar 

  • Vadez V, Deshpande SP, Kholova J, Hammer GL, Borrell AK, Talwar HS, Hash CT (2011) Stay green quantitative trait loci’s effects on water extraction, transpiration efficiency and seed yield depend on recipient parent background. Funct Plant Biol 38:553–566

    Article  Google Scholar 

  • Vadez V, Deshpande S, Kholova J, Ramu P, Hash CT, Varshney R Tuberosa R. (2013) Molecular breeding for stay-green: progress and challenges in sorghum. In: Translational Genomics for Crop Breeding: Abiotic Stress, Yield and Quality, Wiley, New York, pp 125–141

  • Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang SY (2011) Genome‐wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Biol 53:212–231

  • Wang Z, Xu Y, Chen T, Zhang H, Yang J, Zhang J (2015) Abscisic acid and the key enzymes and genes in sucrose-to-starch conversion in rice spikelets in response to soil drying during grain filling. Planta 241:1091–1107

    Article  CAS  Google Scholar 

  • Yan K, Liu P, Wu CA, Yang GD, Xu R, Guo QH, Huang JG, Zheng CC (2012) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48:521–531

    Article  CAS  Google Scholar 

  • Yang YZ, Tan BC (2014) A distal ABA responsive element in AtNCED3 promoter is required for positive feedback regulation of ABA biosynthesis in Arabidopsis. PLoS One 9:e87283

    Article  Google Scholar 

  • Yang J, Zhang J (2006) Grain filling of cereals under soil drying. New Phytol 169:223–236

    Article  CAS  Google Scholar 

  • Yang JC, Zhang JH, Wang ZQ, Zhu QS, Liu LJ (2004) Activities of fructan- and sucrose-metabolizing enzymes in wheat stems subjected to water stress during grain filling. Planta 220:331–343

  • Zolotarov Y, Stromvik M (2015) De novo regulatory motif discovery identifies significant motifs in promoters of five classes of plant dehydrin genes. PLoS One 10:e0129016

    Article  Google Scholar 

Download references

Acknowledgments

Financial assistance provided by Department of Science and Technology, Government of India, is gratefully acknowledged. SD acknowledges the SNP data shared by the Department of Genomics, ICRISAT, Patancheru, India.

Funding

Financial assistance was provided by Department of Science and Technology, Government of India, under the PURSE (Promotion of University Research and Scientific Excellence) program being implemented at Savitribai Phule Pune University (SB and TG).

Author information

Authors and Affiliations

  1. Department of Botany, Savitribai Phule Pune University, Pune, India

    Tejashree Ghate, Vitthal Barvkar & Sujata Bhargava

  2. Genomics and Molecular Breeding, International Crop Research Institute for Semi-Arid Tropics, Patancheru, India

    Santosh Deshpande

Authors
  1. Tejashree Ghate
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vitthal Barvkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Santosh Deshpande
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sujata Bhargava
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sujata Bhargava.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(DOCX 18 kb)

ESM 2

(DOCX 71 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghate, T., Barvkar, V., Deshpande, S. et al. Role of ABA Signaling in Regulation of Stem Sugar Metabolism and Transport under Post- Flowering Drought Stress in Sweet Sorghum. Plant Mol Biol Rep 37, 303–313 (2019). https://doi.org/10.1007/s11105-019-01157-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-019-01157-2

Keywords

  • Abscisic acid
  • Sugar accumulation
  • Drought stress
  • Hormonal regulation
  • Signaling

Search

Navigation