Sugar metabolism as input signals and fuel for leaf senescence

Jeong-Sik Kim1
1Faculty of Science Education, Jeju National University, Jeju, Republic of Korea

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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 23:185–209

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 66:827–840

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 136:3649–3659

Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942

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 125:1396–1405

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 23:873–894

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 42:567–585

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 172:2132–2153

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 151:339–345

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 11:1253–1266

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 8:864–870

Eastmond PJ, Graham IA (2003) Trehalose metabolism: a regulatory role for trehalose-6-phosphate? Curr Opin Plant Biol 6:231–235

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 29:225–235

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) 12:1–12

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 187:139–147

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 111:345–352

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 278:3978–3990

Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102

Goddijn OJ, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4:315–319

Goldthwaite JJ, Laetsch WM (1967) Regulation of senescence in bean leaf discs by light and chemical growth regulators. Plant Physiol 42:1757–1762

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 64:1–13

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 10:15229–15237

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 419:247–259

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 6:39155

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 3:265

Izumi M, Nakamura S (2018) Chloroplast protein turnover: the influence of extraplastidic processes, including autophagy. Int J Mol Sci 19:828

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 154:1196–1209

Jamar C, du Jardin P, Fauconnier ML (2011) Cell wall polysaccharides hydrolysis of malting barley (Hordeum vulgare L.): a review. Biotechnol Agron Soc Environ 15:301–313

Jang JC, León P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19

Khudairi AK (1970) Chlorophyll degradation by light in leaf discs in the presence of sugar. Physiol Plant 23:613–622

Kim J, Woo HR, Nam HG (2016) Toward systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research. Mol Plant 9:813–825

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 7:3193

Kim J, Kim JH, Lyu JI, Woo HR, Lim PO (2018a) New insights into the regulation of leaf senescence in Arabidopsis. J Exp Bot 69:787–799

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 69:3023–3036

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 21:334–346

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 186:58–69

Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807

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 48:405–413

Leopold AC (1961) Senescence in plant development: the death of plants or plant parts may be of positive ecological or physiological value. Science 134:1727–1732

Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125

Lim PO, Nam HG (2005) The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Curr Top Dev Biol 67:49–83

Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 138:2280–2291

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 397:139–148

Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567

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 8:250

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 163:1142–1163

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 211:510–518

Matsoukas IG, Massiah AJ, Thomas B (2013) Starch metabolism and antiflorigenic signals modulate the juvenile-to-adult phase transition in Arabidopsis. Plant Cell Environ 36:1802–1811

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 99:6422–6427

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 138:346–355

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 300:332–336

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 24:463–481

Munne-Bosch S (2008) Do perennials really senesce? Trends Plant Sci 13:216–220

Noh YS, Amasino RM (1999) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41:181–194

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 162:1720–1732

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 12:527–535

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 38:1032–1038

Ono K, Terashima I, Watanabe A (1996) Interaction between nitrogen deficit of a plant and nitrogen content in the old leaves. Plant Cell Physiol 37:1083–1089

Otegui MS (2018) Vacuolar degradation of chloroplast components: autophagy and beyond. J Exp Bot 69:741–750

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 222:989–1000

Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci 73:2781–2807

Polge C, Thomas M (2007) SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci 12:20–28

Poovaiah B (1974) Formation of callose and lignin during leaf abscission. Am J Bot 61:829–834

Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

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 24:4850–4874

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 65:3915–3925

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 173:1017–1030

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:e00669

Seluzicki A, Burko Y, Chory J (2017) Dancing in the dark: darkness as a signal in plants. Plant Cell Environ 40:2487–2501

Shi L, Wu Y, Sheen J (2018) TOR signaling in plants: conservation and innovation. Development 145:dev160887

Silver DM, Kötting O, Moorhead GBG (2014) Phosphoglucan phosphatase function sheds light on starch degradation. Trends Plant Sci 19:471–478

Smith AM, Zeeman SC, Thorneycroft D, Smith SM (2003) Starch mobilization in leaves. J Exp Bot 54:577–583

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 2:1233–1246

Streb S, Zeeman SC (2012) Starch metabolism in Arabidopsis. Arabidopsis Book 10:e0160

Thimann KV, Tetley RM, Krivak BM (1977) Metabolism of oat leaves during senescence: V. Senescence in light. Plant Physiol 59:448–454

Thomas H (2013) Senescence, ageing and death of the whole plant. New Phytol 197:696–711

Thomas H, Stoddart JL (1980) Leaf senescence. Annu Rev Plant Phys 31:83–111

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 59:1963–1972

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 3:406–419

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 13:673–683

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 149:885–893

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 339:704–707

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 162:1290–1310

Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886

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 10:545–554

Wingler A (2018) Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiol 176:1075–1084

Wingler A, Marès M, Pourtau N (2004) Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytol 161:781–789

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 57:391–399

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 158:1241–1251

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 171:452–467

Xie Q, Michaeli S, Peled-Zehavi H, Galili G (2015) Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci 20:264–265

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 42:535–546

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 156:479–490

Yoshida S (2003) Molecular regulation of leaf senescence. Curr Opin Plant Biol 6:79–84

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 149:1860–1871