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Sugar metabolism as input signals and fuel for leaf senescence

  • Jeongsik KimEmail author
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Abstract

Senescence in plants is an active and acquired developmental process that occurs at the last developmental stage during the life cycle of a plant. Leaf senescence is a relatively slow process, which is characterized by loss of photosynthetic activity and breakdown of macromolecules, to compensate for reduced energy production. Sugars, major photosynthetic assimilates, are key substrates required for cellular respiration to produce intermediate sources of energy and reducing power, which are known to be essential for the maintenance of cellular processes during senescence. In addition, sugars play roles as signaling molecules to facilitate a wide range of developmental processes as metabolic sensors. However, the roles of sugar during the entire period of senescence remain fragmentary. The purpose of the present review was to examine and explore changes in production, sources, and functions of sugars during leaf senescence. Further, the review explores the current state of knowledge on how sugars mediate the onset or progression of leaf senescence. Progress in the area would facilitate the determination of more sophisticated ways of manipulating the senescence process in plants and offer insights that guide efforts to maintain nutrients in leafy plants during postharvest storage.

Keywords

Cell wall hydrolase Glucose Leaf senescence Starch Sugar Trehalose-6-phosphate 

Abbreviations

Glc

Glucose

Suc

Sucrose

T6P

Trehalose-6-phosphate

TOR

Target of rapamycin

TPP

Trehalose-6-phosphate phosphatase

TPS

Trehalose-6-phosphate synthase

SnRK1

Sucrose-non-fermenting1-related kinases

SAG

Senescence-associated gene

UDP-Glc

Uridine diphosphate glucose

Notes

Acknowledgements

I apologize to all authors whose studies are not included in the present review due to space limitations. This research was supported by the National Research Foundation of Korea (NRF) Grant funded by the Ministry of Science and ICT (MSIT) (2018R1C1B5086056).

Compliance with ethical standards

Conflict of interest

Author 1 (JK) declares that he has no conflict of interest.

Research involving human and animal rights

This article does not contain any studies with human subjects or animals performed by any of the author.

References

  1. Ahn CS, Han JA, Lee HS, Lee S, Pai HS (2011) The PP2A regulatory subunit Tap46, a component of the TOR signaling pathway, modulates growth and metabolism in plants. Plant Cell 23:185–209CrossRefGoogle Scholar
  2. Ahn CS, Ahn HK, Pai HS (2015) Overexpression of the PP2A regulatory subunit Tap46 leads to enhanced plant growth through stimulation of the TOR signalling pathway. J Exp Bot 66:827–840CrossRefGoogle Scholar
  3. Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659CrossRefGoogle Scholar
  4. Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942CrossRefGoogle Scholar
  5. Blauth SL, Yao Y, Klucinec JD, Shannon JC, Thompson DB, Guilitinan MJ (2001) Identification of mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiol 125:1396–1405CrossRefGoogle Scholar
  6. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D et al (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894CrossRefGoogle Scholar
  7. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Pyung OL, Hong GN, Lin JF, Wu SH, Swidzinski J, Ishizaki K et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585CrossRefGoogle Scholar
  8. Chrobok D, Law SR, Brouwer B, Linden P, Ziolkowska A, Liebsch D, Narsai R, Szal B, Moritz T, Rouhier N et al (2016) Dissecting the metabolic role of mitochondria during developmental leaf senescence. Plant Physiol 172:2132–2153CrossRefGoogle Scholar
  9. Chung BC, Sang Yeb L, Sung Aeong O, Tae Hyong R, Hong Gil N, Lee CH (1997) The promoter activity of sen 1, a senescence-associated gene of Arabidopsis, is repressed by sugars. J Plant Physiol 151:339–345CrossRefGoogle Scholar
  10. Dai N, Schaffer A, Petreikov M, Shahak Y, Giller Y, Ratner K, Levine A, Granot D (1999) Overexpression of arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell 11:1253–1266CrossRefGoogle Scholar
  11. Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M, Bedu M, Robaglia C, Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–870CrossRefGoogle Scholar
  12. Eastmond PJ, Graham IA (2003) Trehalose metabolism: a regulatory role for trehalose-6-phosphate? Curr Opin Plant Biol 6:231–235CrossRefGoogle Scholar
  13. Eastmond PJ, Van Dijken AJH, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JDG, Smeekens SC, Graham IA (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29:225–235CrossRefGoogle Scholar
  14. Evans IM, Rus AM, Belanger EM, Kimoto M, Brusslan JA (2010) Dismantling of Arabidopsis thaliana mesophyll cell chloroplasts during natural leaf senescence. Plant Biol (Stuttg) 12:1–12CrossRefGoogle Scholar
  15. Fröhlich V, Feller U (1991) Effect of phloem interruption on senescence and protein remobilization in the flag leaf of field-grown wheat. Biochem Physiol Pflanz 187:139–147CrossRefGoogle Scholar
  16. Fujiki Y, Yoshikawa Y, Sato T, Inada N, Ito M, Nishida I, Watanabe A (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol Plant 111:345–352CrossRefGoogle Scholar
  17. Ghillebert R, Swinnen E, Wen J, Vandesteene L, Ramon M, Norga K, Rolland F, Winderickx J (2011) The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBS J 278:3978–3990CrossRefGoogle Scholar
  18. Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102CrossRefGoogle Scholar
  19. Goddijn OJ, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4:315–319CrossRefGoogle Scholar
  20. Goldthwaite JJ, Laetsch WM (1967) Regulation of senescence in bean leaf discs by light and chemical growth regulators. Plant Physiol 42:1757–1762CrossRefGoogle Scholar
  21. Gomez LD, Gilday A, Feil R, Lunn JE, Graham IA (2010) AtTPS1-mediated trehalose 6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant J 64:1–13Google Scholar
  22. Guan S, Wang P, Liu H, Liu G, Ma Y, Zhao L (2011) Production of high-amylose maize lines using RNA interference in sbe2a. Afr J Biotechnol 10:15229–15237CrossRefGoogle Scholar
  23. Halford NG, Hey SJ (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419:247–259CrossRefGoogle Scholar
  24. Han Y, Ban Q, Li H, Hou Y, Jin M, Han S, Rao J (2016) DkXTH8, a novel xyloglucan endotransglucosylase/hydrolase in persimmon, alters cell wall structure and promotes leaf senescence and fruit postharvest softening. Sci Rep 6:39155CrossRefGoogle Scholar
  25. Heinrichs L, Schmitz J, Flügge U-I, Häusler R (2012) The mysterious rescue of adg1-1/tpt-2—an Arabidopsis thaliana double mutant impaired in acclimation to high light—by exogenously supplied sugars. Front Plant Sci 3:265CrossRefGoogle Scholar
  26. Izumi M, Nakamura S (2018) Chloroplast protein turnover: the influence of extraplastidic processes, including autophagy. Int J Mol Sci 19:828CrossRefGoogle Scholar
  27. Izumi M, Wada S, Makino A, Ishida H (2010) The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol 154:1196–1209CrossRefGoogle Scholar
  28. Jamar C, du Jardin P, Fauconnier ML (2011) Cell wall polysaccharides hydrolysis of malting barley (Hordeum vulgare L.): a review. Biotechnol Agron Soc Environ 15:301–313Google Scholar
  29. Jang JC, León P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19CrossRefGoogle Scholar
  30. Khudairi AK (1970) Chlorophyll degradation by light in leaf discs in the presence of sugar. Physiol Plant 23:613–622CrossRefGoogle Scholar
  31. Kim J, Woo HR, Nam HG (2016) Toward systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research. Mol Plant 9:813–825CrossRefGoogle Scholar
  32. Kim GD, Cho YH, Yoo SD (2017) Regulatory functions of cellular energy sensor SNF1-related kinase1 for leaf senescence delay through ETHYLENE-INSENSITIVE3 repression. Sci Rep 7:3193CrossRefGoogle Scholar
  33. Kim J, Kim JH, Lyu JI, Woo HR, Lim PO (2018a) New insights into the regulation of leaf senescence in Arabidopsis. J Exp Bot 69:787–799CrossRefGoogle Scholar
  34. Kim J, Park SJ, Lee IH, Chu H, Penfold CA, Kim JH, Buchanan-Wollaston V, Nam HG, Woo HR, Lim PO (2018b) Comparative transcriptome analysis in Arabidopsis ein2/ore3. and ahk3/ore12 mutants during dark-induced leaf senescence. J Exp Bot 69:3023–3036CrossRefGoogle Scholar
  35. Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, Steup M et al (2009) STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21:334–346CrossRefGoogle Scholar
  36. Krapp A, Quick WP, Stitt M (1991) Ribulose-1,5-bisphosphate carboxylase-oxygenase, other Calvin-cycle enzymes, and chlorophyll decrease when glucose is supplied to mature spinach leaves via the transpiration stream. Planta 186:58–69CrossRefGoogle Scholar
  37. Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807CrossRefGoogle Scholar
  38. Lee EJ, Matsumura Y, Soga K, Hoson T, Koizumi N (2007) Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis. Plant Cell Physiol 48:405–413CrossRefGoogle Scholar
  39. Leopold AC (1961) Senescence in plant development: the death of plants or plant parts may be of positive ecological or physiological value. Science 134:1727–1732CrossRefGoogle Scholar
  40. Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125CrossRefGoogle Scholar
  41. Lim PO, Nam HG (2005) The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Curr Top Dev Biol 67:49–83CrossRefGoogle Scholar
  42. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136CrossRefGoogle Scholar
  43. Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 138:2280–2291CrossRefGoogle Scholar
  44. Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajirezaei MR, Stitt M (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397:139–148CrossRefGoogle Scholar
  45. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567CrossRefGoogle Scholar
  46. Lyu JI, Baek SH, Jung S, Chu H, Nam HG, Kim J, Lim PO (2017) High-throughput and computational study of leaf senescence through a phenomic approach. Front Plant Sci 8:250Google Scholar
  47. Martins MC, Hejazi M, Fettke J, Steup M, Feil R, Krause U, Arrivault S, Vosloh D, Figueroa CM, Ivakov A et al (2013) Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol 163:1142–1163CrossRefGoogle Scholar
  48. Masclaux C, Valadier MH, Brugiere N, Morot-Gaudry JF, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211:510–518CrossRefGoogle Scholar
  49. Matsoukas IG, Massiah AJ, Thomas B (2013) Starch metabolism and antiflorigenic signals modulate the juvenile-to-adult phase transition in Arabidopsis. Plant Cell Environ 36:1802–1811CrossRefGoogle Scholar
  50. Menand B, Desnos T, Nussaume L, Bergert F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99:6422–6427CrossRefGoogle Scholar
  51. Mohapatra PK, Patro L, Raval MK, Ramaswamy NK, Biswal UC, Biswal B (2010) Senescence-induced loss in photosynthesis enhances cell wall beta-glucosidase activity. Physiol Plant 138:346–355CrossRefGoogle Scholar
  52. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336CrossRefGoogle Scholar
  53. Moreau M, Azzopardi M, Clément G, Dobrenel T, Marchive C, Renne C, Martin-Magniette M-L, Taconnat L, Renou J-P, Robaglia C et al (2012) Mutations in the Arabidopsis homolog of LST8/GβL, a partner of the target of rapamycin kinase, Impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24:463–481CrossRefGoogle Scholar
  54. Munne-Bosch S (2008) Do perennials really senesce? Trends Plant Sci 13:216–220CrossRefGoogle Scholar
  55. Noh YS, Amasino RM (1999) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41:181–194CrossRefGoogle Scholar
  56. Nunes C, O’Hara LE, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, Paul MJ (2013) The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162:1720–1732CrossRefGoogle Scholar
  57. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12:527–535CrossRefGoogle Scholar
  58. Ono K, Watanabe A (1997) Levels of endogenous sugars, transcripts of rbcS and rbcL, and of RuBisCO protein in senescing sunflower leaves. Plant Cell Physiol 38:1032–1038CrossRefGoogle Scholar
  59. Ono K, Terashima I, Watanabe A (1996) Interaction between nitrogen deficit of a plant and nitrogen content in the old leaves. Plant Cell Physiol 37:1083–1089CrossRefGoogle Scholar
  60. Otegui MS (2018) Vacuolar degradation of chloroplast components: autophagy and beyond. J Exp Bot 69:741–750CrossRefGoogle Scholar
  61. Parrott D, Yang L, Shama L, Fischer AM (2005) Senescence is accelerated, and several proteases are induced by carbon “feast” conditions in barley (Hordeum vulgare L.) leaves. Planta 222:989–1000CrossRefGoogle Scholar
  62. Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci 73:2781–2807CrossRefGoogle Scholar
  63. Polge C, Thomas M (2007) SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci 12:20–28CrossRefGoogle Scholar
  64. Poovaiah B (1974) Formation of callose and lignin during leaf abscission. Am J Bot 61:829–834CrossRefGoogle Scholar
  65. Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282CrossRefGoogle Scholar
  66. Ren M, Venglat P, Qiu S, Feng L, Cao Y, Wang E, Xiang D, Wang J, Alexander D, Chalivendra S et al (2012) Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 24:4850–4874CrossRefGoogle Scholar
  67. Sakuraba Y, Lee SH, Kim YS, Park OK, Hortensteiner S, Paek NC (2014) Delayed degradation of chlorophylls and photosynthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing. J Exp Bot 65:3915–3925CrossRefGoogle Scholar
  68. Sampedro J, Valdivia ER, Fraga P, Iglesias N, Revilla G, Zarra I (2017) Soluble and membrane-bound β-glucosidases are involved in trimming the xyloglucan backbone. Plant Physiol 173:1017–1030CrossRefGoogle Scholar
  69. Scialdone A, Mugford ST, Feike D, Skeffington A, Borrill P, Graf A, Smith AM, Howard M (2013) Arabidopsis plants perform arithmetic division to prevent starvation at night. eLife 2:e00669CrossRefGoogle Scholar
  70. Seluzicki A, Burko Y, Chory J (2017) Dancing in the dark: darkness as a signal in plants. Plant Cell Environ 40:2487–2501CrossRefGoogle Scholar
  71. Shi L, Wu Y, Sheen J (2018) TOR signaling in plants: conservation and innovation. Development 145:dev160887CrossRefGoogle Scholar
  72. Silver DM, Kötting O, Moorhead GBG (2014) Phosphoglucan phosphatase function sheds light on starch degradation. Trends Plant Sci 19:471–478CrossRefGoogle Scholar
  73. Smith AM, Zeeman SC, Thorneycroft D, Smith SM (2003) Starch mobilization in leaves. J Exp Bot 54:577–583CrossRefGoogle Scholar
  74. Stettler M, Eicke S, Mettler T, Messerli G, Hortensteiner S, Zeeman SC (2009) Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol Plant 2:1233–1246CrossRefGoogle Scholar
  75. Streb S, Zeeman SC (2012) Starch metabolism in Arabidopsis. Arabidopsis Book 10:e0160CrossRefGoogle Scholar
  76. Thimann KV, Tetley RM, Krivak BM (1977) Metabolism of oat leaves during senescence: V. Senescence in light. Plant Physiol 59:448–454CrossRefGoogle Scholar
  77. Thomas H (2013) Senescence, ageing and death of the whole plant. New Phytol 197:696–711CrossRefGoogle Scholar
  78. Thomas H, Stoddart JL (1980) Leaf senescence. Annu Rev Plant Phys 31:83–111CrossRefGoogle Scholar
  79. van Doorn WG (2008) Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? J Exp Bot 59:1963–1972CrossRefGoogle Scholar
  80. Vandesteene L, Ramon M, Le Roy K, Van Dijck P, Rolland F (2010) A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol Plant 3:406–419CrossRefGoogle Scholar
  81. Vogel G, Aeschbacher RA, Muller J, Boller T, Wiemken A (1998) Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J 13:673–683CrossRefGoogle Scholar
  82. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149:885–893CrossRefGoogle Scholar
  83. Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–707CrossRefGoogle Scholar
  84. Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162:1290–1310CrossRefGoogle Scholar
  85. Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886CrossRefGoogle Scholar
  86. Weise SE, Aung K, Jarou ZJ, Mehrshahi P, Li Z, Hardy AC, Carr DJ, Sharkey TD (2012) Engineering starch accumulation by manipulation of phosphate metabolism of starch. Plant Biotechnol J 10:545–554CrossRefGoogle Scholar
  87. Wingler A (2018) Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiol 176:1075–1084CrossRefGoogle Scholar
  88. Wingler A, Marès M, Pourtau N (2004) Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytol 161:781–789CrossRefGoogle Scholar
  89. Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57:391–399CrossRefGoogle Scholar
  90. Wingler A, Delatte TL, O’Hara LE, Primavesi LF, Jhurreea D, Paul MJ, Schluepmann H (2012) Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158:1241–1251CrossRefGoogle Scholar
  91. Woo HR, Koo HJ, Kim J, Jeong H, Yang JO, Lee IH, Jun JH, Choi SH, Park SJ, Kang B et al (2016) Programming of plant leaf senescence with temporal and inter-organellar coordination of transcriptome in Arabidopsis. Plant Physiol 171:452–467CrossRefGoogle Scholar
  92. Xie Q, Michaeli S, Peled-Zehavi H, Galili G (2015) Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci 20:264–265CrossRefGoogle Scholar
  93. Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42:535–546CrossRefGoogle Scholar
  94. Yandeau-Nelson MD, Laurens L, Shi Z, Xia H, Smith AM, Guiltinan MJ (2011) Starch-branching enzyme IIa is required for proper diurnal cycling of starch in leaves of maize. Plant Physiol 156:479–490CrossRefGoogle Scholar
  95. Yoshida S (2003) Molecular regulation of leaf senescence. Curr Opin Plant Biol 6:79–84CrossRefGoogle Scholar
  96. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinasel activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149:1860–1871CrossRefGoogle Scholar

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© The Genetics Society of Korea 2019

Authors and Affiliations

  1. 1.Faculty of Science EducationJeju National UniversityJejuRepublic of Korea

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