Skip to main content

Drought stress condition increases root to shoot ratio via alteration of carbohydrate partitioning and enzymatic activity in rice seedlings

Abstract

To understand the underlying mechanism for plasticity in root to shoot ratio (R/S) in response to drought stress, two rice cultivars, Zhenshan97 (drought susceptible) and IRAT109 (drought resistant), were grown hydroponically, and R/S, carbohydrate concentration and partitioning, and activities of enzymes for sucrose conversion in seedlings exposed to drought stress condition (DS) imposed by polyethylene glycol 6000 were investigated. The R/S significantly increased under DS in comparison with that under well-watered condition. The proportion of dry matter and soluble sugar of roots markedly increased under DS. The R/S was negatively correlated with proportion of soluble sugar in stems, and positively with the proportions of soluble sugar and starch in roots. Drought stress condition significantly increased leaf sucrose-phosphate synthase (EC 2.4.1.14) activity and root acid and neutral/alkaline invertase (EC 3.2.1.26) activity. The R/S was positively correlated with leaf sucrose-phosphate synthase and root acid invertase activity, and negatively with leaf sucrose synthase activity in the cleavage direction. Our results indicate that the increase in R/S in response to DS is closely associated with the higher proportion of dry matter and soluble sugar in roots, and this occurs via an increase in leaf sucrose-phosphate synthase and root invertase activity, and thus more sucrose is available for transport from leaves to roots.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

DS:

Drought stress condition

InvA:

Acid invertase

InvN:

Neutral/alkaline invertase

R/S:

Root to shoot ratio

SPS:

Sucrose-phosphate synthase

SSc:

Sucrose synthase in the cleavage direction

SSs:

Sucrose synthase in the synthesis direction

WW:

Well-watered condition

References

  • Asch F, Dingkuhn M, Sow A, Audebert A (2005) Drought-induced changes in rooting patterns and assimilate partitioning between root and shoot in upland rice. Field Crop Res 93:223–236

    Article  Google Scholar 

  • Azhiri-Sigari TA, Yamauchi A, Kamoshita A, Wade LJ (2000) Genotypic variation in response of rainfed lowland rice to drought would help to elucidate how rooting depth and deep root and rewatering II. Root growth. Plant Prod Sci 3:180–188

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cui KH, Huang JL, Xing YZ, Yu SB, Xu CG, Peng SB (2008) Mapping QYLs for seedling characteristics under different water supply conditions in rice (Oryza sativa). Physiol Plant 132:53–68

    CAS  PubMed  Google Scholar 

  • Déjardin A, Sokolov LN, Kleczkowski LA (1999) Sugar/osmoticum levels modulate differential abscisic acid-independent expression of two stress-responsive sucrose synthase genes in Arabidopsis. Biochem J 344:503–509

    Article  PubMed Central  PubMed  Google Scholar 

  • Ericsson T (1995) Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil 168–169:205–214

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 201:502–518

    Article  CAS  Google Scholar 

  • Gowda VRP, Henry A, Yamauchi A, Shashidhar HE, Serraj R (2011) Root biology and genetic improvement for drought avoidance in rice. Field Crop Res 122:1–13

    Article  Google Scholar 

  • Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu MH, Chen ZhL, Qu LJ, Gu HY (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–286

    Article  CAS  PubMed  Google Scholar 

  • Hammond JP, White PJ (2011) Sugar signaling in root response to low phosphorus availability. Plant Physiol 156:1033–1040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hirai G, Chujo H, Tanaka O, Okumura T, Takeuchi S (1994) Studies on the effect of relative humidity of the atmosphere on growth and physiology of rice plants. IX. Effects of water stresses induced by low humidity and the addition of polyethylene glycol to the medium on growth. Jpn J Crop Sci 63:265–270

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ji KX, Wang YY, Sun WN, Lou QJ, Mei HW, Shen SH, Chen H (2012) Drought-responsive mechanisms in rice genotypes with contrasting drought tolerance during reproductive stage. J Plant Physiol 169:336–344

    Article  CAS  PubMed  Google Scholar 

  • Kathiresan A, Lafitte HR, Chen JX, Mansueto L, Bruskiewich R, Bennett J (2006) Gene expression microarrays and their application in drought stress research. Field Crop Res 97:102–110

    Article  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  PubMed  Google Scholar 

  • Lemoine R, Camera SL, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Thévenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci. doi:10.3389/fpls.2013.00272

    Google Scholar 

  • Li ZM, Palmer WM, Martin AP, Wang RQ, Rainsford F, Jin Y, Patrick JW, Yang YJ, Ruan YL (2012) High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit. J Exp Bot 63:1155–1166

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu HS, Li FM, Xu H (2004) Deficiency of water can enhance root respiration rate of drought-sensitive but not drought-tolerant spring wheat. Agr Water Manage 64:41–48

    Article  Google Scholar 

  • Lou Y, Gou JY, Xue HW (2007) PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 19:163–181

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lowell CA, Tomlinson PT, Koch KE (1989) Sucrose-metabolizing enzymes in transport tissues and adjacent sink structures in developing citrus fruit. Plant Physiol 90:1394–1402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophy 444:139–158

    Article  CAS  Google Scholar 

  • Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2011) Plant phenotypic plasticity in a changing climate. Trends in Plant Sci 15:684–692

    Article  Google Scholar 

  • Pavlinova OA, Balakhontsev EN, Prasolova MF, Turkina MV (2002) Sucrose-phosphate synthase, sucrose synthase, and invertase in sugar beet leaves. Russ J Plant Physiol 49:69–73

    Article  Google Scholar 

  • Pinheiro C, Chaves MM, Ricardo CP (2001) Alterations in carbon and nitrogen metabolism induced by water deficit in the stems and leaves of Lupinus albus L. J Exp Bot 52:1063–1070

    Article  CAS  PubMed  Google Scholar 

  • Poorter H, Niklas K, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50

    Article  CAS  PubMed  Google Scholar 

  • Rich SM, Watt M (2013) Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. J Exp Bot 64:1193–1208

    Article  CAS  PubMed  Google Scholar 

  • Roitsch T, Gonzalez MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613

    Article  CAS  PubMed  Google Scholar 

  • Sergeeva LI, Keurentjes JJB, Bentsink L, Vonk J, van der Plas LHW, Koornneef M, Vreugdenhil D (2006) Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. P Natl Acad Sci USA 103:2994–2999

    Article  CAS  Google Scholar 

  • Shone MGT, Whipps JM, Flood AV (1983) Effects of localized and overall water stress on assimilate partitioning in barley between shoots, roots and root exudates. New Phytol 95:625–634

    Article  CAS  Google Scholar 

  • Slama I, Messedi D, Ghnaya T, Savoure A, Abdelly C (2006) Effects of water deficit on growth and proline metabolism in Sesuvium portulacastrum. Environ Exp Bot 56:231–238

    Article  CAS  Google Scholar 

  • 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 11:177–189

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tripathy JN, Zhang JX, Robin S, Nguyen TT, Nguyen HT (2000) QTLs for cell-membrane stability mapped in rice (Oryza sativa L.) under drought stress. Theor Appl Genet 100:1197–1202

    Article  CAS  Google Scholar 

  • Vargas WA, Pontis HG, Salerno GL (2007) Differential expression of alkaline and neutral invertases in response to environmental stresses: characterization of an alkaline isoform as a stress-response enzyme in wheat leaves. Planta 226:1535–1545

    Article  CAS  PubMed  Google Scholar 

  • Wang HG, Zhang HL, Li ZC (2007) Analysis of gene expression profile induced by water stress in upland rice (Oryza sativa L. var. IRAT109) seedlings using subtractive expressed sequence Tags library. J Integr Plant Biol 49:1455–1463

    Article  CAS  Google Scholar 

  • Wilson JB (1988) A review of evidence on the control of shoot: root ratio, in relation to models. Ann Bot 61:433–449

    Google Scholar 

  • Wind J, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochemistry 71:1610–1614

    Article  CAS  PubMed  Google Scholar 

  • Wissuwa M, Gamat G, Ismail AM (2005) Is root growth under phosphorus deficiency affected by source or sink limitations? J Exp Bot 56:1943–1950

    Article  CAS  PubMed  Google Scholar 

  • Yang JC, Zhang JH, Wang ZQ, Zhu QS (2001) Activities of starch hydrolytic enzymes and sucrose-phosphate synthase in the stems of rice subjected to water stress during grain filling. J Exp Bot 52:2169–2179

    CAS  PubMed  Google Scholar 

  • Yoshida S, Forno DA, Cook JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. International Rice Research Institute, Manila

    Google Scholar 

  • Yue B, Xue WY, Xiong LZ, Yu XQ, Luo LJ, Cui KH, Jin DM, Xing YZ, Zhang QF (2006) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172:1213–1228

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou J, Wang X, Jiao Y, Qin Y, Liu X, He K, Chen C, Ma L, Wang J, Xiong L, Zhang Q, Fan L, Deng XW (2007) Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol Biol 63:591–608

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu YJ, Komor E, 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  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was jointly supported by Key Projects in the National Science & Technology Pillar Program from the Ministry of Science and Technology (2013BAD07B10) and by Research Fund for the Doctoral Program of Higher Education from the Ministry of Education (20110146110021).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kehui Cui.

Additional information

Communicated by W. Filek.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Xu, W., Cui, K., Xu, A. et al. Drought stress condition increases root to shoot ratio via alteration of carbohydrate partitioning and enzymatic activity in rice seedlings. Acta Physiol Plant 37, 9 (2015). https://doi.org/10.1007/s11738-014-1760-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-014-1760-0

Keywords

  • Carbohydrate partitioning
  • Invertase
  • Rice (Oryza sativa L)
  • Root to shoot ratio
  • Sucrose-phosphate synthase
  • Drought stress condition