Advertisement

Expression analysis of genes associated with sucrose accumulation and its effect on source–sink relationship in high sucrose accumulating early maturing sugarcane variety

  • I. Verma
  • K. Roopendra
  • A. Sharma
  • A. Chandra
  • A. Kamal
Research Article
  • 9 Downloads

Abstract

Sucrose synthesis/accumulation in sugarcane depends on the source–sink communication wherein source responds to sink demand for photoassimilate supply. Sucrose in stalk (sink) acts as signal, and sends feedback to restrain further synthesis of sucrose by regulating photosynthetic efficiency of leaves (source). Hence sucrose synthesis/accumulation is controlled by many genes and regulatory sequences including 3 invertases (SAI, CWI, NI), sucrose synthase (SuSy) and sucrose phosphate synthase (SPS). SPS and invertase play key role in enhancing sink strength which ultimately promotes greater sucrose accumulation in the sink tissues. In present study, a significant positive correlation was found between sucrose% of source and sink tissues which was greater in the top (R2= 0.679) than middle (R2= 0.580) and bottom (R2= 0.518) internodes, depicting that sucrose accumulation in the stalk bears a direct relation with sucrose translocation efficiency from source. Results indicated an increased sucrose% with maturity, while reducing sugar content decreased with crop growth. qRT-PCR results exhibited an elevated expression of invertase in immature sink tissues depicting increased sink requirement, which declined with maturity. Similarly, increased PEP carboxylase gene expression as observed supported the fact that higher sink demand results in enhanced photosynthetic rate and thus influences the source activity. SPS was found active at initial stage of cane development indicating its role in sucrose synthesis. Thus by studying expression patterns of the different genes both, in source and sink tissues, a better understanding of the sucrose accumulation pathway in sugarcane is possible, which in turn can help in elucidating ways to enhance sucrose concentration in sink.

Keywords

Source–sink qRT-PCR Sucrose accumulation Sink strength Sink demand 

Notes

Acknowledgements

Authors are thankful to ICAR-Indian Institute of Sugarcane Research, Lucknow and Integral University, Lucknow for providing necessary facilities and guidance to carry out this work. IV thankful to Integral University for providing manuscript ID (IU/R&D/2018-MCN000393). Authors are thankful to the anonymous reviewer for critical review and improvement.

Compliance with ethical standards

Conflict of interest

All the authors declare that they have no conflicts of interest.

References

  1. Albertson PL, Peters KF, Grof CPL (2001) An improved method for the measurement of cell wall invertase activity in sugarcane tissue. Funct Plant Biol 28:323–328CrossRefGoogle Scholar
  2. Ap Rees T (1987) Compartmentation of plant metabolism. In: Davies DD (ed) The biochemistry of plants, 12th edn. Academic Press, San Diego, pp 87–115Google Scholar
  3. Barratt DHP, Barber L, Kruger NJ, Smith AM, Wang TL, Martin C (2001) Multiple distinct isoforms of sucrose synthase in pea. Plant Physiol 127:655–664CrossRefPubMedPubMedCentralGoogle Scholar
  4. Berding N (1997) Clonal improvement of sugarcane based on selection for moisture content: fact or fiction. Proc Aust Soc Sugarcane Technol 19:245–253Google Scholar
  5. Bosch S, Grof CPL, Botha FC (2004) Expression of neutral invertase in sugarcane. Plant Sci 166:1125–1133CrossRefGoogle Scholar
  6. Buczynski SR, Thom M, Chourey P, Maretzki A (1993) Tissue distribution and characterization of sucrose synthase isozymes in sugarcane. J Plant Physiol 142:641–646CrossRefGoogle Scholar
  7. Bull TA, Glasziou KT (1963) The evolutionary significance of sugar accumulation in Saccharum. Aust J Biol Sci 16:737–742CrossRefGoogle Scholar
  8. Chandra A (2011) Physio-biochemical and molecular approaches to enhance sucrose content in sugarcane: Indian initiatives. Sugar Tech 13:315–321CrossRefGoogle Scholar
  9. Chandra A, Jain R, Rai RK, Solomon S (2011) Revisiting the source–sink paradigm in sugarcane. Curr Sci 100:978–980Google Scholar
  10. Chandra A, Jain R, Solomon S (2012) Complexities of invertases controlling sucrose accumulation and retention in sugarcane: the way forward. Curr Sci 102:857–866Google Scholar
  11. 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 17:608–617CrossRefPubMedGoogle Scholar
  12. Franck N, Vaast P, Ge´nard M, Dauzat J (2006) Soluble sugars mediate sink feedback down-regulation of leaf photosynthesis in field-grown Coffea arabica. Tree Physiol 26:517–525CrossRefPubMedGoogle Scholar
  13. Gayler KR, Glasziou KT (1972) Storage of sugars in stalks of sugarcane. Bot Rev 38:471–490CrossRefGoogle Scholar
  14. Geigenberger P, Stitt M (1993) Sucrose synthase catalyzes a rapidly reversible reaction in vivo in developing potato tubers and other plant tissues. Planta 189:329–339CrossRefPubMedGoogle Scholar
  15. Grof CPL, Campbell JA (2001) Sugarcane sucrose metabolism: scope for molecular manipulation. Aust J Plant Physiol 28:1–12Google Scholar
  16. 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 47:1530–1539CrossRefGoogle Scholar
  17. Gutierrez-Miceli FA, Rodriguez-Mendiola MA, Ochoa-Alejo N, Mendez-Salas R, Dendooven L, Arias-Castro C (2002) Relationship between sucrose accumulation and activities of sucrose-phosphatase, sucrose synthase, neutral invertase and soluble acid invertase in micropropagated sugarcane plants. Acta Physiol Plant 24:441–446CrossRefGoogle Scholar
  18. Hammond JBW, Burton KS, Shaw AF, Ho LC (1984) Source—sink relationships and carbon metabolism in tomato leaves 2. carbohydrate pools and catabolic enzymes. Ann Bot 53:307–314CrossRefGoogle Scholar
  19. 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 38:344–348CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hibberd JM, Covshoff S (2010) The regulation of gene expression required for C4 photosynthesis. Annu Rev Plant Biol 61:181–207CrossRefPubMedGoogle Scholar
  21. Hubbard NI, Huber SC, Pharr DM (1989) Sucrose phosphate synthase and acid invertase as determinants of sucrose concentration in developing muskmelon (Cucumis melo L.) fruits. Plant Physiol 91:1527–1534CrossRefPubMedPubMedCentralGoogle Scholar
  22. Inman-Bamber NG, Bonnett GD, Spillman MF, Hewitt ML, Jackson J (2008) Increasing sucrose accumulation in sugarcane by manipulating leaf extension and photosynthesis with irrigation. Aust J Agric Res 59:13–26CrossRefGoogle Scholar
  23. 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 22:325–337CrossRefGoogle Scholar
  24. Jackson PA (2005) Breeding for improved sugar content in sugarcane. Field Crops Res 92:277–290CrossRefGoogle Scholar
  25. Jacobsen KR, Fisher DG, Maretzki A, Moore PH (1992) Developmental changes in the anatomy of the sugarcane stem in relation to phloem unloading and sucrose storage. Plant Biol 105:70–80Google Scholar
  26. Jeschke WD, Hilpert A (1997) Sink-stimulated photosynthesis and sink-dependent increase in nitrate uptake: nitrogen and carbon relations of the parasitic association Cuscutareflexa-Ricinus communis. Plant, Cell Environ 20:47–56CrossRefGoogle Scholar
  27. Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant, Cell Environ 26:37–56CrossRefGoogle Scholar
  28. Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Thévenot P, Maurousset L, Faucher M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:1–21CrossRefGoogle Scholar
  29. Lian L, Wang X, Zhu Y, He W, Cai Q, Xie H, Zhang M, Zhang J (2014) Physiological and photosynthetic characteristics of indica Hang2 expressing the sugarcane PEPC gene. Mol Biol Rep 41:2189–2197CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lingle SE (1999) Sugar metabolism during growth and development in sugarcane internodes. Crop Sci 39:480–486CrossRefGoogle Scholar
  31. Lingle SE, Smith RC (1991) Sucrose metabolism related to growth and ripening in sugarcane internodes. Crop Sci 31:172–177CrossRefGoogle Scholar
  32. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  33. Marcelis LFM (1996) Sink strength as a determinant of dry matter partitioning in the whole plant. J Exp Bot 47:1281–1291CrossRefPubMedGoogle Scholar
  34. McCormick AJ, Cramer MD, Watt DA (2006) Sink strength regulates photosynthesis in sugarcane. New Phytol 171:759–770CrossRefPubMedGoogle Scholar
  35. McCormick AJ, Cramer MD, Watt DA (2008) Culm sucrose accumulation promotes physiological decline of mature leaves in ripening sugarcane. Fields Crops Res 108:250–258CrossRefGoogle Scholar
  36. McCormick AJ, Watt DA, Cramer MD (2009) Supply and demand: sink regulation of sugar accumulation in sugarcane. J Exp Bot 60:357–364CrossRefPubMedGoogle Scholar
  37. Moore PH (1995) Temporal and spatial regulation of sucrose accumulation in the sugarcane stem. Aust J Plant Physiol 22:661–679Google Scholar
  38. Moore PH, Botha FC, Furbank RT (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, Wallinford, UKGoogle Scholar
  39. Nelson N (1944) A photometric adaptation of Somogyi method for the determination of glucose. J Biol Chem 153:375–380Google Scholar
  40. Nonis A, Ruperti B, Falchi R, Casatta E, Thamasebi Enferadi S, Vizzotto G (2007) Differential expression and regulation of a neutral invertase encoding gene from peach (Prunus persica): evidence for a role in fruit development. Physiol Plant 129:436–446CrossRefGoogle Scholar
  41. Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1381–1400CrossRefGoogle Scholar
  42. Rae AL, Perroux JM, Grof CPL (2005) Sucrose partitioning between vascular bundles and storage parenchyma in the sugarcane stem: a potential role for the ShSUT1 sucrose transporter. Planta 220:817–825CrossRefPubMedGoogle Scholar
  43. Roitsch T, Bittne M, Godt DE (1995) Induction of apoplastic invertase of Chenopodium rubrum by d-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol 108:285–294CrossRefPubMedPubMedCentralGoogle Scholar
  44. Roitsch T, Balibrea ME, Hofmann M, Proels R, Singh AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524CrossRefPubMedGoogle Scholar
  45. Ruan YL, Chourey PS (2006) Carbon partitioning in developing seed. In: Basra AS (ed) Seed sciences and technology: trends and advances. The Haworth Press, New York, pp 125–152Google Scholar
  46. Stitt M, Gerhardt R, Wilke I, Heldt HW (1987) The contribution of fructose 2, 6-bisphosphate to the regulation of sucrose synthesis during photosynthesis. Physiol Plant 69:377–386CrossRefGoogle Scholar
  47. Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–8CrossRefPubMedPubMedCentralGoogle Scholar
  48. Tang GQ, Lüscher M, Sturm A (1999) Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11:177–189CrossRefPubMedPubMedCentralGoogle Scholar
  49. Tejera NA, Rodés R, Ortega E, Campos R, Lluch C (2007) Comparative analysis of physiological characteristics and yield components in sugarcane cultivars. Field Crops Resh 102:64–72CrossRefGoogle Scholar
  50. Van Handel E (1968) Direct micro determination of sucrose. Anal Biochem 22:280–283CrossRefPubMedGoogle Scholar
  51. Verma I, Roopendra K, Sharma A, Jain R, Singh RK, Chandra A (2017) Expression analysis of genes associated with sucrose accumulation in sugarcane under normal and GA3-induced source–sink perturbed conditions. Acta Physiol Planta 39:133CrossRefGoogle Scholar
  52. Watt DA, McCormick AJ, Govender C, Carson DL, Cramer MD, Huckett BI, Botha FC (2005) Increasing the utility of genomics in unraveling sucrose accumulation. Field Crops Res 92:149–158CrossRefGoogle Scholar
  53. Welbaum GE, Meinzer FC, Grayson RL, Thornham KT (1992) Evidence for the consequences of a barrier to solute diffusion between the apoplast and vascular bundles in sugarcane stalk tissue. Funct Plant Biol 19:611–623CrossRefGoogle Scholar
  54. 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 115:609–616CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2018

Authors and Affiliations

  1. 1.Division of Plant Physiology and BiochemistryICAR-Indian Institute of Sugarcane ResearchLucknowIndia
  2. 2.Department of BiosciencesIntegral UniversityLucknowIndia

Personalised recommendations