Influence of High Temperature on Sucrose Metabolism in Chalky and Translucent Rice Genotypes

  • K. P. Sharma
  • N. SharmaEmail author
Research Article


Chalk is an unwanted and unpleasant opaque area in the rice grain caused by loosely packed starch granules possessing numerous air spaces. High temperature during grain filling favours induction of chalky grains; therefore, studying grain sink activity and carbon partitioning under these conditions would help to elucidate the difference in sucrose metabolism in chalky and translucent genotypes. Two rice genotypes viz., PAU-3699-13-2-1-1 (chalky) and PR122 (translucent) were sown at two different dates in order to expose the plants to different temperature regimes during grain filling. Significant increase in sucrose content, reduction in sucrose synthase (SuSy) and increased acid invertase (AIV) activity was observed during early transplanting (ET) when the crop encountered heat stress. Reduction in SuSy activity during ET did not allow cleavage of sucrose, thereby restricting the synthesis of starch. PAU-3699-13-2-1-1 exhibited higher acid invertase activity than PR122. The partially purified AIV exhibited optimum pH of 5.5 and 5.0 during ET, but 5.0 and 4.5 during normal transplanting (NT) in PAU-3699-13-2-1-1 and PR 122, respectively. The optimum temperature for AIV activity was 50 and 45 °C for the two genotypes during ET and NT, respectively. Changes in optimum pH, optimum temperature and Km of AIV during ET might be responsible for reduced accumulation of starch and increase in percent of chalky grains. Enhanced AIV activity may enable the grain carbon metabolism to adapt to high temperatures by providing hexoses for enhanced respiratory needs experienced during grain development.


Rice grains Transplanting dates Sucrose synthase Acid invertase Heat stress Chalk 



The authors are thankful to Dr. G. S. Mangat, Sr. Rice Breeder—cum–Incharge for providing the necessary facilities and Dr. R. Kaur, Plant Breeder, for helping in carrying out field experiments. The authors declare that they have no conflict of interest.

Supplementary material

40011_2017_865_MOESM1_ESM.doc (42 kb)
Supplementary material 1 (DOC 42 kb)


  1. 1.
    Singh N, Singh J, Kaur L, Sodhi NS, Gill BS (2003) Morphological thermal and rheological properties of starches from different botanical sources. Food Chem 81:219–231CrossRefGoogle Scholar
  2. 2.
    Fitzgerald MA, Resurreccion AP (2009) Maintaining the yield of edible rice in a warming world. Funct Plant Biol 36:1037CrossRefGoogle Scholar
  3. 3.
    Lanning SB, Siebenmorgen TJ, Counce PA, Ambardekar AA, Mauromoustakos A (2011) Extreme nighttime air temperatures in 2010 impact rice chalkiness and milling quality. Field Crops Res 124:132–136CrossRefGoogle Scholar
  4. 4.
    Crowley TJ (2000) Causes of climate change over the past 1000 years. Sci 289:270–277CrossRefGoogle Scholar
  5. 5.
    Coast O, Ellis RH, Murdoch AJ, Quinones C, Jagadish KSV (2015) High night temperature induces contrasting responses for spikelet fertility, spikelet tissue temperature, flowering characteristics and grain quality in rice. Funct Plant Biol 42:149–161CrossRefGoogle Scholar
  6. 6.
    Cao YY, Chen YH, Chen MX, Wang ZQ, Wu CF, Bian XC, Yang JC, Zhang JH (2016) Growth characteristics and endosperm structure of superior and inferior spikelets of indica rice under high-temperature stress. Biol Plant 1:11Google Scholar
  7. 7.
    Suwa R, Hakata H, Hara H, El-Shemy HA, Adu-Gyamfi JJ, Nguyen NT, Kanai S, Lightfoot DA, Mohapatra PK, Fujita K (2010) High temperature effects on photosynthate partitioning and sugar metabolism during ear expansion in maize (Zea mays L.) genotypes. Plant Physiol Biochem 48:124–130CrossRefPubMedGoogle Scholar
  8. 8.
    Zinn KE, Tunc OM, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Wang L, Lu Q, Wen X, Lu C (2015) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–2862PubMedPubMedCentralGoogle Scholar
  10. 10.
    Liang J, Zhang J, Cao X (2001) Grain sink strength may be related to the poor grain filling of indica-japonica rice (Oryza sativa) hybrids. Physiol Plant 112:470–477CrossRefPubMedGoogle Scholar
  11. 11.
    Asthir B, Rai PK, Bains NS, Sohu SS (2012) Genotypic variation for high temperature tolerance in relation to carbon partitioning and grain sink activity in wheat. Am J Plant Sci 3:381–390CrossRefGoogle Scholar
  12. 12.
    Tian LI, Qi LH, Ryu Ohsugi, Yamagishi T, Sasaki H (2006) Effect of high temperature on sucrose content and sucrose cleaving enzyme activity in rice grain during the filling stage. Rice Sci 13:205–210Google Scholar
  13. 13.
    Kato T (1995) Change of sucrose synthase activity in developing endosperm of rice cultivars. Crop Sci 35:827–831CrossRefGoogle Scholar
  14. 14.
    Shankar T, Thangamathi P, Rama R, Sivakumar T (2014) Characterization of invertase from Sacchromyces cervisiae MTCC 170. Afr J Microbio Res 8:1385–1393CrossRefGoogle Scholar
  15. 15.
    Eschrich W (1980) Free space invertase, its possible role in phloem unloading. Ber Dtsch Bot Ges 93:363–378Google Scholar
  16. 16.
    Gibeaut DM, Karuppiah N, Chang SR, Brock TG, Vadlamudi B, Kim D, Ghosheh NS, Rayle DL, Carpita NC, Kaufman PB (1990) Cell wall and enzyme changes during graviresponse of the leaf-sheat pulvinus of oat (Avena sativa). Plant Physiol 94:411–416CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–7CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Pollock CJ, Lloyd EJ (1977) The distribution of acid invertase in developing leaves of Lolium temulentum L. Planta 133:197–200CrossRefPubMedGoogle Scholar
  19. 19.
    Sebkova V, Unger C, Hardegger M, Sturm A (1995) Biochemical, physiological and molecular characterisation of sucrose synthase from Daucus carota. Plant Physiol 108:75–83CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth, and carbon partitioning. Trends Plant Sci 4:401–440CrossRefPubMedGoogle Scholar
  21. 21.
    Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Biochem Mol Biol 35:253–289CrossRefPubMedGoogle Scholar
  22. 22.
    Van Handel E (1968) Direct micro determination of sucrose. Anal Biochem 22:280–283CrossRefPubMedGoogle Scholar
  23. 23.
    Kerr PS, Kalt-Torres W, Huber SC (1987) Resolution of two molecular forms of sucrose-phosphate synthase from maize, soybean and spinach leaves. Planta 170:515–519CrossRefPubMedGoogle Scholar
  24. 24.
    Nelson N (1944) A photometric adaptation of somogyi method for the determination of glucose. J Biol Chem 153:375–380Google Scholar
  25. 25.
    Bradford MN (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  26. 26.
    Lineweaver H, Burk D (1934) Determination of enzyme dissociation constants. J Am Chem Soc 56:658–666CrossRefGoogle Scholar
  27. 27.
    Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  28. 28.
    Keeling PL, Banisadr R, Barone L, Wasserman BP, Singletary GW (1994) Effect of temperature on enzymes in the pathway of starch biosynthesis in developing wheat and maize grain. Aust J Plant Physiol 21:807–827CrossRefGoogle Scholar
  29. 29.
    Lisle AJ, Martin M, Fitzgerald MA (2000) Chalky and translucent rice grains differ in starch composition and structure and cooking properties. Cereal Chem 77:627–632CrossRefGoogle Scholar
  30. 30.
    Tanamachi K, Miyazaki M, Matsuo K, Suriyasak C, Tamada A, Matsuyama K, Iwaya-Inoue M, Ishibashi Y (2016) Differential responses to high temperature during maturation in heat-stress-tolerant cultivars of Japonica rice. Plant Prod Sci 19:300–308CrossRefGoogle Scholar
  31. 31.
    Ehness R, Ecker M, Godt DE, Roitsch T (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9:1825–1841CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524CrossRefPubMedGoogle Scholar
  33. 33.
    Yang J, Zhang J, Wang Z, Xu G, Zhu Q (2004) Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiol 135:1621–1629CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lemoine R, Camera SL, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Théveno PC, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source- to—sink transport of sugar and regulation by environmental factors. Frontier Plant Sci Plant Physiol 4:1–21Google Scholar
  35. 35.
    Geigenberger P, Reimholz R, Geiger M, Merlo L, Canale V, Stitt M (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short—term water deficit. Planta 201:502–518CrossRefGoogle Scholar
  36. 36.
    Liu CC, Huang LC, Chang CT, Sung HY (2006) Purification and characterization of soluble invertases from suspension-cultured bamboo (Bambusa edulis) cells. Food Chem 96:621–631CrossRefGoogle Scholar
  37. 37.
    Isla MI, Salerno G, Pontis H, Vattuone MA, Sampietro AR (1995) Purification and properties of the soluble acid invertase from Oryza sativa. Phytochem 38:321–325CrossRefGoogle Scholar
  38. 38.
    Ashraf H, Aftab ZH (2015) Biosynthesis, partial purification and characterization of invertase through Carrot (Daucus carota L.) Peels. Acad J Biotech 3(15):25. doi: 10.15413/ajb.2014.0113 CrossRefGoogle Scholar
  39. 39.
    Akardere E, Ozer B, Celemand EB, Secil OS (2010) Three-phase partitioning of Invertase from Baker’s yeast. Sep Purif Technol 72:35–339CrossRefGoogle Scholar
  40. 40.
    Guimaraes LHS, Somera AF, Terenzi HF, Polizeli MT, Jorge JA (2009) Production of β-fructofuranosidases by Aspergillus niveus using agro-industrial residues as carbon sources: characterization of an intracellular enzyme accumulated in the presence of glucose. Process Biochem 44:237–241CrossRefGoogle Scholar
  41. 41.
    Uma C, Gomathi D, Ravikumar G, Kalaiselvi M, Palaniswamy M (2012) Production and properties of invertase from a Cladosporium cladosporioides in SmF using pomegranate peel waste as substrate. Asian Pac J Trop Biomed 2:S605–S611CrossRefGoogle Scholar
  42. 42.
    Lin CL, Lin HC, Wang AY, Sung HY (1999) Purification and characterization of an alkaline invertase from shoots of etiolated rice seedlings. New Phytol 142:427–434CrossRefGoogle Scholar

Copyright information

© The National Academy of Sciences, India 2017

Authors and Affiliations

  1. 1.Department of BiochemistryPunjab Agricultural UniversityLudhianaIndia
  2. 2.Department of Plant Breeding and GeneticsPunjab Agricultural UniversityLudhianaIndia

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