Skip to main content
Log in

Expression analysis of genes associated with sucrose accumulation in sugarcane under normal and GA3-induced source–sink perturbed conditions

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Sugarcane accumulates high amount of sucrose, thus making it one of the important cash crops worldwide. The final destination of sucrose accumulation in sugarcane is sink tissue, i.e., stalk, supplied by the source, i.e., leaf, to fulfill the need of plant growth, respiration, storage, and other metabolic activities. Signals between sink and source tissues regulate sucrose accumulation in sink and possibly the negative feedback from the sink restrains further accumulation in the stalk. However, perturbation of this negative feedback may help to improve sugar yield. This can be achieved by the application of GA3 (Gibberellic acid), a plant growth regulator, known to excite physiological responses and modify the source–sink metabolism through their effect on photosynthesis, which in turn improves sink strength by redistribution of the photoassimilates. In the present study, GA3 applied canes showed prominent increase in invertase activity, at early stage of the application, to provide hexoses. This in turn helped increase the internodal length and cane capacity for additional accumulation of sucrose, thereby increasing sink strength. At maturity, sucrose% and brix% were found higher in middle and top portions of the GA3-applied canes. Expression analysis of various sucrose metabolising genes viz., sucrose phosphate synthase (SPS), sucrose synthase (SuSy), soluble acid invertase, neutral invertase, and cell wall invertase (CWI) was carried out at different growth stages, using quantitative RT-PCR. CWI, which plays key role in phloem unloading in sink tissues, exhibited higher expression in GA3 samples at the elongation stage which decreased with maturity, whereas both SuSy and SPS, involved in regulation of sucrose accumulation, showed a variable level of expression. Thus, GA3 application on cane may improve the sucrose content in stalk and thus assuage maneuvering source–sink dynamics in sugarcane.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

CWI:

Cell wall invertase

GA3 :

Gibberellic acid

NI:

Neutral invertase

SAI:

Soluble acid invertase

SPS:

Sucrose phosphate synthase

SuSy:

Sucrose synthase

qRT-PCR:

Quantitative reverse transcriptase PCR

References

  • Aloni B, Daie J, Wyse RE (1986) Enhancement of [14C] sucrose export from source leaves of Vicia faba by gibberellic acid. Plant Physiol 82:962–966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batta SK, Singh R (1986) Sucrose metabolism in sugarcane grown under varying climatic conditions: synthesis and storage of sucrose in relation to the activities of sucrose synthase, sucrose phosphate synthase and invertase. Phytochemistry 25:2431–2437

    Article  CAS  Google Scholar 

  • Bosch S, Grof CPL, Botha FC (2004) Expression of neutral invertase in sugarcane. Plant Sci 166:1125–1133

    Article  CAS  Google Scholar 

  • Botha FC, Black KG (2000) Sucrose phosphate synthase and sucrose synthase activity during maturation of intermodal tissue in sugarcane. Aust J Plant Physiol 27:81–85

    CAS  Google Scholar 

  • Botha FC, Sawyer BJB, Birch RG (2001) Sucrose metabolism in the culm of transgenic sugarcane with reduced soluble acid invertase activity. Proc Intl Soc Sugar Cane Technol 24:588–591

    Google Scholar 

  • Botha FC, Lakshmanan P, O’Connell A, Moore PH (2013) Hormones and growth regulators. In: Moore PH, Botha FC (eds) Sugarcane: physiology, biochemistry, and functional biology. Wiley, Chichester, pp 331–377. doi:10.1002/9781118771280

    Chapter  Google Scholar 

  • Buczynski SR, Thom M, Chourey P, Maretzki A (1993) Tissue distribution and characterization of sucrose synthase isozymes in sugarcane. J Plant Physiol 142:641–646

    Article  CAS  Google Scholar 

  • Bull TA, Glasziou KT (1963) The evolutionary significance of sugar accumulation in Saccharum. Aust J Biol Sci 16:737–742

    Article  CAS  Google Scholar 

  • Buren LL, Moore PH, Yamasaki Y (1979) Gibberellin studies with sugarcane. II. Hand-sampled field trials. Crop Sci 19:425–428

    Article  CAS  Google Scholar 

  • Burg SP, Bieleski RL (1962) The physiology of sugarcane. V. Kinetics of sugar accumulation. Aust J Biol Sci 15:429–444

    Article  Google Scholar 

  • Chandra A, Jain R, Solomon S (2012) Complexities of invertases controlling sucrose accumulation and retention in sugarcane: the way forward. Curr Sci 102:857–866

    CAS  Google Scholar 

  • Chandra A, Verma PK, Islam MN, Grisham MP, Jain R, Sharma A, Roopendra K, Singh K, Singh P, Verma I, Solomon S (2015) Expression analysis of genes associated with sucrose accumulation in sugarcane (Saccharum spp. hybrids) varieties differing in content and time of peak sucrose storage. Plant Biol 17:608–617

    Article  CAS  PubMed  Google Scholar 

  • Cheikh N, Brenner ML, Huber JL, Huber SC (1992) Regulation of sucrose phosphate synthase by gibberellins in soybean and spinach plants. Plant Physiol 100:1238–1242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WS, Liu ZH, Yang L, Chen WH (1994) Gibberellin and temperature influence carbohydrate content and flowering in Phalaenopsis. Physiol Plant 90:391–395

    Article  CAS  Google Scholar 

  • Cheng WH, Taliercio EW, Chourey PS (1996) The Miniaturel seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8:971–983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiou TJ, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci 95:4784–4788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clowes M (1980) Growth stimulation from ethrel and the effects of gibberellic acid when applied to sugarcane. Proc South Afr Sugar Technol Assoc 49:146–150

    Google Scholar 

  • Cole DF, Dobrenz AK, Massengale MA (1972) Effect of gibberellic acid on alfalfa (Medicago sativa L.). Crop Sci 12:674–676

    Article  CAS  Google Scholar 

  • Davies PJ (1995) Plant hormones, physiology, biochemistry and molecular biology. Kluwer, Dordrecht

    Google Scholar 

  • Doehlert DC, Huber SC (1985) The role of sulphahydryl groups in the regulation of spinach leaf sucrose phosphate synthase. Biochem Biophys Acta 93:353–355

    Google Scholar 

  • Eschrich W (1980) Free space invertase, its possible role in phloem unloading. Berichte der Deutschen Botanischem Gesellschaft 93:363–378

    CAS  Google Scholar 

  • Farrar JF (1993) Sink strength: what is it and how do we measure it? Introduction. Plant Cell Environ 16:10–15

    Google Scholar 

  • Farrar J (1996) Regulation of shoot-root ratio is mediated by sucrose. Plant Soil 185:13–19

    Article  CAS  Google Scholar 

  • Gayler KR, Glasziou KT (1972) Storage of sugars in stalks of sugarcane. Bot Rev 38:471–490

    Article  Google Scholar 

  • Geigenberger P, Stitt M (1993) Sucrose synthase catalyses a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta 189:329–339

    Article  CAS  PubMed  Google Scholar 

  • Giaquinta RT (1979) Sucrose translocation and storage in the sugar beet. Plant Physiol 63:828–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102

    Article  CAS  PubMed  Google Scholar 

  • Goldner W, Thom M, Maretzki A (1991) Sucrose metabolism in sugarcane cell suspension cultures. Plant Sci 73:143–147

    Article  Google Scholar 

  • Groenewald JH, Botha FC (2007) Down-regulation of pyrophosphate: fructose 6- phosphate1-phosphotransferase (PFP) activity in sugarcane enhances sucrose accumulation in immature internodes. Transg Res 17:85–92

    Article  Google Scholar 

  • Grof CPL, Albertson PL, Bursle J, Perroux JM, Bonnett GD, Manners JM (2007) Sucrose-phosphate synthase, a biochemical marker of high sucrose accumulation in sugarcane. Crop Sci 47:1530–1539

    Article  CAS  Google Scholar 

  • Hänggi E, Fleming AJ (2001) Sucrose synthase expression pattern in young maize leaves: implications for phloem transport. Planta 214:326–329

    PubMed  Google Scholar 

  • Hatch MD, Glasziou KT (1963) Sugar accumulation cycle in sugarcane. II. Relationship of invertase activity to sugar content and growth rate in storage tissue of plants growth in controlled environments. Plant Physiol 38:344–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann-Thoma G, Hinkel K, Nicolay P, Willenbrink J (1996) Sucrose accumulation in sweet sorghum stem internodes in relation to growth. Physiol Plant 97:277–284

    Article  CAS  Google Scholar 

  • Huang D, Qin C, Gui Y, Zhao L, Chen Z, Wang M, Sun Y, Liao Q, Li Y, Lakshmanan P (2017) Role of the SPS gene families in the regulation of sucrose accumulation in sugarcane. Sugar Tech 19:117–124

    Article  CAS  Google Scholar 

  • Huber SC, Akazawa T (1986) A novel sucrose synthase pathway for sucrose degradation in cultured sycamore cells. Plant Physiol 81:1008–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huber SC, Huber JL (1996) Role and regulation of sucrose phosphate synthase in higher plants. Ann Rev Plant Physiol Plant Mol Biol 47:431–444

    Article  CAS  Google Scholar 

  • Iqbal N, Nazar R, Khan MIR, Masood A, Khan NA (2011) Role of gibberellins in regulation of source–sink relations under optimal and limiting environmental conditions. Curr Sci 100:998–1007

    CAS  Google Scholar 

  • Iskandar HM, Simpson RS, Casu RE, Bonnett GD, Maclean DJ, Manners JM (2004) Comparison of reference genes for quantitative real-time polymerase chain reaction analysis of gene expression in sugarcane. Plant Mol Biol Rep 22:325–337

    Article  CAS  Google Scholar 

  • Jackson PA (2005) Breeding for improved sugar content in sugarcane. Field Crops Resh 92:277–290

    Article  Google Scholar 

  • Jain R, Chandra A, Solomon S (2013) Impact of exogenously applied enzyme effectors on sucrose metabolizing enzymes (SPS, SS and SAI) and sucrose content in sugarcane. Sugar Tech 5:370–378

    Article  Google Scholar 

  • Kaufman PB, Ghosheh NS, LaCroix JD, Soni SL, Ikuma H (1973) Regulation of invertase levels in Avena stem segments by gibberellic acid, sucrose, glucose, and fructose. Plant Physiol 52:221–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan NA, Singh S, Nazar R, Lone PM (2007) The source–sink relationship in mustard. Asian Aust J Plant Sci Biotech 1:10–18

    Google Scholar 

  • Kozłowska M, Rybus-Zając M, Stachowiak J, Janowska B (2007) Changes in carbohydrate contents of Zantedeschia leaves under gibberellin-stimulated flowering. Acta Physiol Plant 29:27–32

    Article  Google Scholar 

  • Krapp A, Hofman B, Schäfer C, Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates:mechanism for the sink regulation of photosynthesis? Plant J 3:817–828

    Article  CAS  Google Scholar 

  • Lakshmanan P, Geijskes RJ, Aitken KS, Grof CLP, Bonnet GD, Smith GR (2005) Sugarcane biotechnology: the challenges and opportunities. In Vitro Cell Dev Biol Plant 41:345–363

    Article  CAS  Google Scholar 

  • Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugar and amino acids. Plant Cell Environ 26:37–56

    Article  CAS  Google Scholar 

  • Lingle SE, Smith RC (1991) Sucrose metabolism related to growth and ripening in sugarcane internodes. Crop Sci 31:172–177

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lunn JE, Furbank RT (1999) Sucrose biosynthesis in C4 plants. New Phytol 143:221–237

    Article  CAS  Google Scholar 

  • McCormick AJ, Cramer MD, Watt D (2006) Sink strength regulates photosynthesis in sugarcane. New Phytol 171:759–770

    Article  CAS  PubMed  Google Scholar 

  • McCormick AJ, Watt DA, Cramer MD (2009) Supply and demand: sink regulation of sugar accumulation in sugarcane. J Exp Bot 60:357–364

    Article  CAS  PubMed  Google Scholar 

  • Miller EM, Chourey PS (1992) The maize invertase-deficient miniature-l seed mutant is associated with aberrant pedicel and endosperm development. Plant Cell 4:297–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore PH (1977) Use of gibberellic acid to increase sugarcane yields in Hawaii. Proc Plant Growth Regul Work Group 4:173–180

    CAS  Google Scholar 

  • Moore PH (1995) Temporal and spatial regulation of sucrose metabolism in the sugarcane stem. Aust J Plant Physiol 22:661–679

    Article  CAS  Google Scholar 

  • Moore PH, Buren LL (1978) Gibberellin studies with sugarcane. I. Cultivar differences in growth responses to gibberellic acid. Crop Sci 17:443–446

    Article  Google Scholar 

  • Moore PH, Ginoza H (1980) Gibberellin studies with sugarcane. III. Effects of rate and frequency of gibberellic acid applications on stalk length and fresh weight. Crop Sci 20:78–82

    Article  Google Scholar 

  • Moore PH, Botha FC, Furbank RT, Grof CPL (1997) Potential for overcoming physio-biochemical limits to sucrose accumulation. In: Keating BA, Wilson JR (eds) Intensive sugarcane production: meeting the challenges beyond 2000. CAB International, Wallingford, pp 141–155

    Google Scholar 

  • Morris DA, Arthur ED (1985) Effects of gibberellic acid on patterns of carbohydrate distribution and acid invertase activity in Phaseolus vulgaris. Physiol Plant 65:257–262

    Article  CAS  Google Scholar 

  • Nelson N (1944) A photometric adaptation of Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    CAS  Google Scholar 

  • Nguyen-Quoc B, Foyer CH (2001) A role for “futile cycles” involving invertase and sucrose synthase metabolism of tomato fruit. J Exp Bot 52:881–889

    Article  CAS  PubMed  Google Scholar 

  • Ranwala AP, Miller WB (2008) Gibberellin-mediated changes in carbohydrate metabolism during flower stalk elongation in tulips. Plant Growth Regul 55:241–248

    Article  CAS  Google Scholar 

  • Sacher JA, Hatch MD, Glasziou KT (1963) Sugar accumulation cycle in sugarcane. III. Physical and metabolic aspect of cycle in immature storage tissues. Plant Physiol 39:348–354

    Article  Google Scholar 

  • Schafer WE, Rohwer JM, Botha FC (2004) Protein level expression and localization of sucrose synthase in sugarcane culm. Physiol Plant 121:187–195

    Article  PubMed  Google Scholar 

  • Uys L, Botha FC, Hofmeyr JHS, Rohwer JM (2007) Kinetic model of sucrose accumulation in maturing sugarcane culm tissue. Phytochemistry 68:2375–2392

    Article  CAS  PubMed  Google Scholar 

  • Verma AK, Upadhyaya SK, Srivastava MK, Verma PC, Solomon S, Singh SB (2011) Transcript expression and soluble acid invertase during sucrose accumulation in sugarcane. Acta Physiol Plant 33:1749–1757

    Article  CAS  Google Scholar 

  • Walsh KB, Sky RC, Brown SM (2005) The anatomy of the pathway of sucrose unloading within the sugarcane stalk. Funct Plant Biol 32:367–374

    Article  CAS  Google Scholar 

  • Whittaker A, Botha FC (1997) Carbon partitioning during sucrose accumulation in sugarcane internodal tissue. Plant Physiol 115:1651–1659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, Birch RG (2007) Doubling sugar content in sugarcane plants modified to produce a sucrose isomer. Plant Biotech J 5:109–117

    Article  CAS  Google Scholar 

  • Wu L, Mitchell JP, Cohn NS, Kaufman PB (1993) Gibberellin (GA3) enhances cell wall invertase activity and mRNA levels in elongating dwarf pea (Pisum sativum) shoots. Int J Plant Sci 154:280–289

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Tanabe K, Tamura F, Itai A, Yoshida M (2007) Roles of gibberellins in increasing sink demand in Japanese pear fruit during rapid fruit growth. Plant Growth Regul 52:161–172

    Article  CAS  Google Scholar 

  • Zhu YJ, Albert HH, Moore PH (1997) Sucrose accumulation in the sugarcane stem is regulated by the difference between the activities of soluble acid invertase and sucrose phosphate synthase. Plant Physiol 115:609–616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Science and Engineering Research Board (SERB/SR/SO/PS/36/2012), Department of Science and Technology, Government of India. Authors are also thankful to the Director for necessary facilities to carry out the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Chandra.

Additional information

Communicated by O. Ferrarese-Filho.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Verma, I., Roopendra, K., Sharma, A. et al. Expression analysis of genes associated with sucrose accumulation in sugarcane under normal and GA3-induced source–sink perturbed conditions. Acta Physiol Plant 39, 133 (2017). https://doi.org/10.1007/s11738-017-2433-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-017-2433-6

Keywords

Navigation