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Sucrose is involved in the regulation of iron deficiency responses in rice (Oryza sativa L.)

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Sucrose signaling pathways were rapidly induced in response to early iron deficiency in rice plants, and the change of sucrose contents in plants was essential for the activation of iron deficiency responses.

Abstract

Sucrose is the main product of photosynthesis in plants, and it functions not only as an energy metabolite but also a signal molecule. However, a few studies have examined the involvement of sucrose in mediating iron deficiency responses in rice. In this study, we found that the decrease in photosynthesis and total chlorophyll concentration (SPAD values) in leaves occurred at a very early stage under iron deficiency. In addition, the sucrose was increased in leaves but decreased in roots of rice plants under iron deficiency, and also the sucrose transporter (SUT) encoded genes’ expression levels in leaves were all inhibited, including OsSUT1, OsSUT2, OsSUT3, OsSUT4, and OsSUT5. The carbohydrate distribution was changed under iron deficiency and sucrose might be involved in the iron deficiency responses of rice plants. Furthermore, exogenous application of sucrose or dark treatment experiments were used to test the hypothesis; we found that the increased endogenous sucrose would cause the repression of iron acquisition-related genes in roots, while further stimulated iron transport-related genes in leaves. Compared to the exogenous application of sucrose, the dark treatment had the opposite effects. All the above results highlighted the important role of sucrose in regulating the responses of rice plants to iron deficiency.

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References

  • Aoki N, Hirose T, Scofield GN et al (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232

    Article  CAS  PubMed  Google Scholar 

  • Bashir K, Inoue H, Nagasaka S et al (2006) Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J Biol Chem 281:32395–32402

    Article  CAS  PubMed  Google Scholar 

  • Briat JF, Fobis-Loisy I, Grignon N et al (1995) Cellular and molecular aspects of iron metabolism in plants. Biol Cell 84:69–81

    Article  CAS  Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994a) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250

    Article  CAS  Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994b) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. J Exp Bot 45:1251–1257

    Article  CAS  Google Scholar 

  • Chen L, Zhao X, Ding C et al (2014) Physiological and molecular responses under Fe deficiency in two rice (Oryza sativa) genotypes differing in iron accumulation ability in seeds. J Plant Growth Regul 33:769–777

    Article  CAS  Google Scholar 

  • Cheng L, Wang F, Shou H et al (2007) Mutation in nicotianamine aminotransferase stimulated the Fe (II) acquisition system and led to iron accumulation in rice. Plant Physiol 145:1647–1657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciereszko I, Barbachowska A (2000) Sucrose metabolism in leaves and roots of bean (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 156:640–644

    Article  CAS  Google Scholar 

  • Ciereszko I, Gniazdowska A, Mikulska M et al (1996) Assimilate translocation in bean plants (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 149:343–348

    Article  CAS  Google Scholar 

  • Conte SS, Walker EL (2011) Transporters contributing to iron trafficking in plants. Mol Plant 4:464–476

    Article  CAS  PubMed  Google Scholar 

  • Dasgupta K, Khadilkar AS, Sulpice R et al (2014) Expression of sucrose transporter cDNAs specifically in companion cells enhances phloem loading and long-distance transport of sucrose but leads to an inhibition of growth and the perception of a phosphate limitation. Plant Physiol 165:715–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eide D, Broderius M, Fett J et al (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci 93:5624–5628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enomoto Y, Hodoshima H, Shimada H et al (2007) Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots. Planta 227:81–89

    Article  CAS  PubMed  Google Scholar 

  • García MJ, Romera FJ, Stacey MG et al (2013) Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants. Planta 237:65–75

    Article  PubMed  Google Scholar 

  • Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109

    Article  CAS  PubMed  Google Scholar 

  • Inoue H, Kobayashi T, Nozoye T et al (2009) Rice OsYSL15 is an iron-regulated iron (III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the plants. J Biol Chem 284:3470–3479

    Article  CAS  PubMed  Google Scholar 

  • Karthikeyan AS, Varadarajan DK, Jain A et al (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Ann Rev Plant Biol 63:131–152

    Article  CAS  Google Scholar 

  • Kobayashi T, Itai RN, Nishizawa NK (2014) Iron deficiency responses in rice roots. Rice 7:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Kobayashi T, Itai RN, Senoura T et al (2016) Jasmonate signaling is activated in the very early stages of iron deficiency responses in rice roots. Plant Mol Biol 91:533–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koike S, Inoue H, Mizuno D et al (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39:415–424

    Article  CAS  PubMed  Google Scholar 

  • Lambers H, Chapin IIIFS., Pons TL (1998) Photosynthesis, respiration, and long-distance transport. Springer, New York

    Book  Google Scholar 

  • Lee S, Chiecko JC, Kim SA et al (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin XY, Ye YQ, Fan SK et al (2016) Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signaling in Arabidopsis plants. Plant physiology 170:907–920

    Article  CAS  PubMed  Google Scholar 

  • Ling HQ, Bauer P, Bereczky Z et al (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci 99(21):13938–13943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Samac DA, Bucciarelli B et al (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41:257–268

    Article  CAS  PubMed  Google Scholar 

  • Liu DD, Chao WM, Turgeon R (2012) Transport of sucrose, not hexose, in the phloem. J Exp Bot 63(11):4315–4320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Liang X, Zhou F et al (2017) Accessing the agronomic and photosynthesis-related traits of high-yielding winter wheat mutants induced by ultra-high pressure. Field Crops Res 213:165–173

    Article  Google Scholar 

  • Morcuende R, Bari R, Gibon Y et al (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    Article  CAS  PubMed  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL et al (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694

    Article  CAS  PubMed  Google Scholar 

  • Romera FJ, Alcántara E (2004) Ethylene involvement in the regulation of Fe-deficiency stress responses by strategy I plants. Funct Plant Biol 31:315–328

    Article  CAS  Google Scholar 

  • Schmidt W, Schuck C (1996) Pyridine nucleotide pool size changes in iron-deficient Plantago lanceolata roots during reduction of external oxidants. Physiol Plant 98:215–221

    Article  CAS  Google Scholar 

  • Vert GA, Briat JF, Curie C (2003) Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol 132:796–804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Li G, Zhang WH (2015) Brassinosteroids are involved in Fe homeostasis in rice (Oryza sativa L.). J Exp Bot 66:2749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Wei H, Xue Z et al (2017) Gibberellins regulate iron deficiency-response by influencing iron transport and translocation in rice plants (Oryza sativa). Annals of botany 119:945–956

    Article  PubMed  PubMed Central  Google Scholar 

  • Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 19:31–67

    Article  CAS  Google Scholar 

  • Wu J, Wang C, Zheng L et al (2011) Ethylene is involved in the regulation of iron homeostasis by regulating the expression of iron-acquisition-related genes in Oryza sativa. J Exp Bot 62:667–674

    Article  CAS  PubMed  Google Scholar 

  • Yokosho K, Yamaji N, Ueno D et al (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149:297–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Forno DA, Cock JH (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute

  • Zakhleniuk OV, Raines CA, Lloyd JC (2001) pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. Planta 212:529–534

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Science Foundation of Jiangsu Province (Grants No. BK20160716), Jiangsu Collaborative Innovation Center for Modern Crop Production, the Ministry of National Science and Technology of China (2013BAD07B09), and the National Key Research and Development Program of China (2017YFD0301200).

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Correspondence to Lin Chen or Yan-Feng Ding.

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Communicated by Prakash Lakshmanan.

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Chen, PF., Chen, L., Jiang, ZR. et al. Sucrose is involved in the regulation of iron deficiency responses in rice (Oryza sativa L.). Plant Cell Rep 37, 789–798 (2018). https://doi.org/10.1007/s00299-018-2267-8

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