GROWTH REGULATING FACTOR5 stimulates Arabidopsis chloroplast division, photosynthesis, and leaf longevity

. 2015 Mar ; 167 (3) : 817-32. [epub] 20150120

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25604530

Arabidopsis (Arabidopsis thaliana) leaf development relies on subsequent phases of cell proliferation and cell expansion. During the proliferation phase, chloroplasts need to divide extensively, and during the transition from cell proliferation to expansion, they differentiate into photosynthetically active chloroplasts, providing the plant with energy. The transcription factor GROWTH REGULATING FACTOR5 (GRF5) promotes the duration of the cell proliferation period during leaf development. Here, it is shown that GRF5 also stimulates chloroplast division, resulting in a higher chloroplast number per cell with a concomitant increase in chlorophyll levels in 35S:GRF5 leaves, which can sustain higher rates of photosynthesis. Moreover, 35S:GRF5 plants show delayed leaf senescence and are more tolerant for growth on nitrogen-depleted medium. Cytokinins also stimulate leaf growth in part by extending the cell proliferation phase, simultaneously delaying the onset of the cell expansion phase. In addition, cytokinins are known to be involved in chloroplast development, nitrogen signaling, and senescence. Evidence is provided that GRF5 and cytokinins synergistically enhance cell division and chlorophyll retention after dark-induced senescence, which suggests that they also cooperate to stimulate chloroplast division and nitrogen assimilation. Taken together with the increased leaf size, ectopic expression of GRF5 has great potential to improve plant productivity.

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Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Mühlenbock P, Skirycz A, Gonzalez N, Beemster GTS, et al. (2012) Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell 22: 64–78 PubMed

Argueso CT, Ferreira FJ, Kieber JJ (2009) Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant Cell Environ 32: 1147–1160 PubMed

Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20: 2102–2116 PubMed PMC

Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108: 1505–1517 PubMed PMC

Baker NR. (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59: 89–113 PubMed

Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55: 1607–1621 PubMed

Beemster GTS, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inzé D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138: 734–743 PubMed PMC

Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang YH, Schaller GE, Loraine A, Kieber JJ (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol 162: 272–294 PubMed PMC

Boonman A, Prinsen E, Gilmer F, Schurr U, Peeters AJM, Voesenek LACJ, Pons TL (2007) Cytokinin import rate as a signal for photosynthetic acclimation to canopy light gradients. Plant Physiol 143: 1841–1852 PubMed PMC

Brenner WG, Ramireddy E, Heyl A, Schmülling T (2012) Gene regulation by cytokinin in Arabidopsis. Front Plant Sci 3: 8. PubMed PMC

Brenner WG, Romanov GA, Köllmer I, Bürkle L, Schmülling T (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J 44: 314–333 PubMed

Chiang YH, Zubo YO, Tapken W, Kim HJ, Lavanway AM, Howard L, Pilon M, Kieber JJ, Schaller GE (2012) Functional characterization of the GATA transcription factors GNC and CGA1 reveals their key role in chloroplast development, growth, and division in Arabidopsis. Plant Physiol 160: 332–348 PubMed PMC

Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20: 503–508 PubMed

Cortleven A, Valcke R (2012) Evaluation of the photosynthetic activity in transgenic tobacco plants with altered endogenous cytokinin content: lessons from cytokinin. Physiol Plant 144: 394–408 PubMed

Coschigano KT, Melo-Oliveira R, Lim J, Coruzzi GM (1998) Arabidopsis gls mutants and distinct Fd-GOGAT genes: implications for photorespiration and primary nitrogen assimilation. Plant Cell 10: 741–752 PubMed PMC

Cutcliffe JW, Hellmann E, Heyl A, Rashotte AM (2011) CRFs form protein-protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain. J Exp Bot 62: 4995–5002 PubMed PMC

D’Agostino IB, Deruère J, Kieber JJ (2000) Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol 124: 1706–1717 PubMed PMC

Debernardi JM, Mecchia MA, Vercruyssen L, Smaczniak C, Kaufmann K, Inze D, Rodriguez RE, Palatnik JF (2014) Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. Plant J 79: 413–426 PubMed

Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706: 12–39 PubMed

Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, et al. (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA 104: 14537–14542 PubMed PMC

Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215: 407–419 PubMed

Dortay H, Gruhn N, Pfeifer A, Schwerdtner M, Schmülling T, Heyl A (2008) Toward an interaction map of the two-component signaling pathway of Arabidopsis thaliana. J Proteome Res 7: 3649–3660 PubMed

Dortay H, Mehnert N, Bürkle L, Schmülling T, Heyl A (2006) Analysis of protein interactions within the cytokinin-signaling pathway of Arabidopsis thaliana. FEBS J 273: 4631–4644 PubMed

Edgerton MD. (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149: 7–13 PubMed PMC

Eloy NB, de Freitas Lima M, Van Damme D, Vanhaeren H, Gonzalez N, De Milde L, Hemerly AS, Beemster GTS, Inzé D, Ferreira PCG (2011) The APC/C subunit 10 plays an essential role in cell proliferation during leaf development. Plant J 68: 351–363 PubMed

Frick G, Su Q, Apel K, Armstrong GA (2003) An Arabidopsis porB porC double mutant lacking light-dependent NADPH:protochlorophyllide oxidoreductases B and C is highly chlorophyll-deficient and developmentally arrested. Plant J 35: 141–153 PubMed

Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270: 1986–1988 PubMed

Gonzalez N, De Bodt S, Sulpice R, Jikumaru Y, Chae E, Dhondt S, Van Daele T, De Milde L, Weigel D, Kamiya Y, et al. (2010) Increased leaf size: different means to an end. Plant Physiol 153: 1261–1279 PubMed PMC

Gutiérrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, et al. (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105: 4939–4944 PubMed PMC

Hedtke B, Alawady A, Albacete A, Kobayashi K, Melzer M, Roitsch T, Masuda T, Grimm B (2012) Deficiency in riboflavin biosynthesis affects tetrapyrrole biosynthesis in etiolated Arabidopsis tissue. Plant Mol Biol 78: 77–93 PubMed

Holst K, Schmülling T, Werner T (2011) Enhanced cytokinin degradation in leaf primordia of transgenic Arabidopsis plants reduces leaf size and shoot organ primordia formation. J Plant Physiol 168: 1328–1334 PubMed

Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43: 68–78 PubMed

Hudson D, Guevara D, Yaish MW, Hannam C, Long N, Clarke JD, Bi YM, Rothstein SJ (2011) GNC and CGA1 modulate chlorophyll biosynthesis and glutamate synthase (GLU1/Fd-GOGAT) expression in Arabidopsis. PLoS ONE 6: e26765. PubMed PMC

Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, et al. (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18: 3073–3087 PubMed PMC

Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413: 383–389 PubMed

Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63: 353–380 PubMed

Ishida K, Yamashino T, Yokoyama A, Mizuno T (2008) Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant Cell Physiol 49: 47–57 PubMed

Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787–799 PubMed

Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62: 1499–1509 PubMed

Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193–195 PubMed

Kawade K, Horiguchi G, Usami T, Hirai MY, Tsukaya H (2013) ANGUSTIFOLIA3 signaling coordinates proliferation between clonally distinct cells in leaves. Curr Biol 23: 788–792 PubMed

Kazama T, Ichihashi Y, Murata S, Tsukaya H (2010) The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. Plant Cell Physiol 51: 1046–1054 PubMed

Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62: 1399–1409 PubMed

Kiba T, Yamada H, Sato S, Kato T, Tabata S, Yamashino T, Mizuno T (2003) The type-A response regulator, ARR15, acts as a negative regulator in the cytokinin-mediated signal transduction in Arabidopsis thaliana. Plant Cell Physiol 44: 868–874 PubMed

Kieber JJ, Schaller GE (2014) Cytokinins. The Arabidopsis Book 12: e0168, doi/10.1199/tab.0168 PubMed PMC

Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci USA 103: 814–819 PubMed PMC

Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36: 94–104 PubMed

Kim JH, Lee BH (2006) GROWTH-REGULATING FACTOR4 of Arabidopsis thaliana is required for development of leaves, cotyledons, and shoot apical meristem. J Plant Biol 49: 463–468

Kim JS, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, Nakashima K, Mitsuda N, Takiguchi Y, Ohme-Takagi M, Kondou Y, et al. (2012) Arabidopsis GROWTH-REGULATING FACTOR7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A. Plant Cell 24: 3393–3405 PubMed PMC

Kobayashi Y, Kanesaki Y, Tanaka A, Kuroiwa H, Kuroiwa T, Tanaka K (2009) Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc Natl Acad Sci USA 106: 803–807 PubMed PMC

Kuijt SJ, Greco R, Agalou A, Shao J, ’t Hoen CC, Overnäs E, Osnato M, Curiale S, Meynard D, van Gulik R, et al. (2014) Interaction between the GROWTH-REGULATING FACTOR and KNOTTED1-LIKE HOMEOBOX families of transcription factors. Plant Physiol 164: 1952–1966 PubMed PMC

Kuroda H, Masuda T, Fusada N, Ohta H, Takamiya K (2000) Expression of NADPH-protochlorophyllide oxidoreductase gene in fully green leaves of cucumber. Plant Cell Physiol 41: 226–229 PubMed

Kusnetsov V, Herrmann RG, Kulaeva ON, Oelmüller R (1998) Cytokinin stimulates and abscisic acid inhibits greening of etiolated Lupinus luteus cotyledons by affecting the expression of the light-sensitive protochlorophyllide oxidoreductase. Mol Gen Genet 259: 21–28 PubMed

Lee DJ, Kim S, Ha YM, Kim J (2008) Phosphorylation of Arabidopsis response regulator 7 (ARR7) at the putative phospho-accepting site is required for ARR7 to act as a negative regulator of cytokinin signaling. Planta 227: 577–587 PubMed

Lee DJ, Park JY, Ku SJ, Ha YM, Kim S, Kim MD, Oh MH, Kim J (2007) Genome-wide expression profiling of ARABIDOPSIS RESPONSE REGULATOR 7 (ARR7) overexpression in cytokinin response. Mol Genet Genomics 277: 115–137 PubMed

Lichtenthaler HK. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148: 350–382

Lillo C. (2008) Signalling cascades integrating light-enhanced nitrate metabolism. Biochem J 415: 11–19 PubMed

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

Liu H, Guo S, Xu Y, Li C, Zhang Z, Zhang D, Xu S, Zhang C, Chong K (2014a) OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol 165: 160–174 PubMed PMC

Liu J, Hua W, Yang HL, Zhan GM, Li RJ, Deng LB, Wang XF, Liu GH, Wang HZ (2012) The BnGRF2 gene (GRF2-like gene from Brassica napus) enhances seed oil production through regulating cell number and plant photosynthesis. J Exp Bot 63: 3727–3740 PubMed PMC

Liu J, Rice JH, Chen N, Baum TJ, Hewezi T (2014b) Synchronization of developmental processes and defense signaling by growth regulating transcription factors. PLoS ONE 9: e98477. PubMed PMC

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods 25: 402–408 PubMed

Lochmanová G, Zdráhal Z, Konecná H, Koukalová S, Malbeck J, Soucek P, Válková M, Kiran NS, Brzobohaty B (2008) Cytokinin-induced photomorphogenesis in dark-grown Arabidopsis: a proteomic analysis. J Exp Bot 59: 3705–3719 PubMed

Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17: 3007–3018 PubMed PMC

Maurino VG, Peterhansel C (2010) Photorespiration: current status and approaches for metabolic engineering. Curr Opin Plant Biol 13: 249–256 PubMed

Mok M. (1994) Cytokinins and plant development: an overview. InMok D, Mok M, eds, Cytokinins: Chemistry, Activity, and Function. CRC Press, Boca Raton, FL, pp 155–166

Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473–497

Naito T, Kiba T, Koizumi N, Yamashino T, Mizuno T (2007) Characterization of a unique GATA family gene that responds to both light and cytokinin in Arabidopsis thaliana. Biosci Biotechnol Biochem 71: 1557–1560 PubMed

Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126: 467–475 PubMed

Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, Matsui M, Nakanishi H, Miyagishima SY (2009) The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21: 1769–1780 PubMed PMC

Oosawa N, Masuda T, Awai K, Fusada N, Shimada H, Ohta H, Takamiya K (2000) Identification and light-induced expression of a novel gene of NADPH-protochlorophyllide oxidoreductase isoform in Arabidopsis thaliana. FEBS Lett 474: 133–136 PubMed

Paddock TN, Mason ME, Lima DF, Armstrong GA (2010) Arabidopsis protochlorophyllide oxidoreductase A (PORA) restores bulk chlorophyll synthesis and normal development to a porB porC double mutant. Plant Mol Biol 72: 445–457 PubMed

Pedersen DS, Coppens F, Ma L, Antosch M, Marktl B, Merkle T, Beemster GT, Houben A, Grasser KD (2011) The plant-specific family of DNA-binding proteins containing three HMG-box domains interacts with mitotic and meiotic chromosomes. New Phytol 192: 577–589 PubMed

Possingham JV, Lawrence ME (1983) Controls to plastid division. Int Rev Cytol 84: 1–56

Procházková D, Haisel D, Wilhelmová N (2008) Antioxidant protection during ageing and senescence in chloroplasts of tobacco with modulated life span. Cell Biochem Funct 26: 582–590 PubMed

Pyke KA, Leech RM (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol 99: 1005–1008 PubMed PMC

Rachmilevitch S, Cousins AB, Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proc Natl Acad Sci USA 101: 11506–11510 PubMed PMC

Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci USA 103: 11081–11085 PubMed PMC

Reinbothe S, Reinbothe C, Lebedev N, Apel K (1996) PORA and PORB, two light-dependent protochlorophyllide-reducing enzymes of angiosperm chlorophyll biosynthesis. Plant Cell 8: 763–769 PubMed PMC

Richter R, Behringer C, Müller IK, Schwechheimer C (2010) The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes Dev 24: 2093–2104 PubMed PMC

Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18: 40–54 PubMed PMC

Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544 PubMed

Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137: 103–112 PubMed PMC

Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11: 440–448 PubMed

Sakamoto W, Miyagishima SY, Jarvis P (2008) Chloroplast biogenesis: control of plastid development, protein import, division and inheritance. The Arabidopsis Book 6: e0110, doi/10.1199/tab.0110 PubMed PMC

Skirycz A, De Bodt S, Obata T, De Clercq I, Claeys H, De Rycke R, Andriankaja M, Van Aken O, Van Breusegem F, Fernie AR, et al. (2010) Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. Plant Physiol 152: 226–244 PubMed PMC

Spano G, Di Fonzo N, Perrotta C, Platani C, Ronga G, Lawlor DW, Napier JA, Shewry PR (2003) Physiological characterization of ‘stay green’ mutants in durum wheat. J Exp Bot 54: 1415–1420 PubMed

Steiner E, Efroni I, Gopalraj M, Saathoff K, Tseng TS, Kieffer M, Eshed Y, Olszewski N, Weiss D (2012) The Arabidopsis O-linked N-acetylglucosamine transferase SPINDLY interacts with class I TCPs to facilitate cytokinin responses in leaves and flowers. Plant Cell 24: 96–108 PubMed PMC

Synková H, Schnablová R, Polanská L, Husák M, Siffel P, Vácha F, Malbeck J, Machácková I, Nebesárová J (2006) Three-dimensional reconstruction of anomalous chloroplasts in transgenic ipt tobacco. Planta 223: 659–671 PubMed

Tanaka R, Kobayashi K, Masuda T (2011) Tetrapyrrole metabolism in Arabidopsis thaliana. The Arabidopsis Book 9: e0145, doi/10.1199/tab.0145 PubMed PMC

Tanaka R, Tanaka A (2011) Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim Biophys Acta 1807: 968–976 PubMed

Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A (2007) ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol 48: 263–277 PubMed

Terry MJ, Smith AG (2013) A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis. Front Plant Sci 4: 14. PubMed PMC

To JPC, Haberer G, Ferreira FJ, Deruère J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16: 658–671 PubMed PMC

Vercruyssen L, Gonzalez N, Werner T, Schmülling T, Inzé D (2011) Combining enhanced root and shoot growth reveals cross talk between pathways that control plant organ size in Arabidopsis. Plant Physiol 155: 1339–1352 PubMed PMC

Vercruyssen L, Verkest A, Gonzalez N, Heyndrickx KS, Eeckhout D, Han SK, Jégu T, Archacki R, Van Leene J, Andriankaja M, et al. (2014) ANGUSTIFOLIA3 binds to SWI/SNF chromatin remodeling complexes to regulate transcription during Arabidopsis leaf development. Plant Cell 26: 210–229 PubMed PMC

Waters MT, Moylan EC, Langdale JA (2008) GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J 56: 432–444 PubMed

Waters MT, Wang P, Korkaric M, Capper RG, Saunders NJ, Langdale JA (2009) GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21: 1109–1128 PubMed PMC

Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15: 2532–2550 PubMed PMC

Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12: 527–538 PubMed

Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death: regulation by multiple layers of control and implications for aging in general. J Cell Sci 126: 4823–4833 PubMed

Wu J, Neimanis S, Heber U (1991) Photorespiration is more effective than the Mehler reaction in protecting the photosynthetic apparatus against photoinhibition. Bot Acta 104: 283–291

Zhang Z, Li G, Gao H, Zhang L, Yang C, Liu P, Meng Q (2012) Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence Zea mays L. inbred lines. PLoS ONE 7: e42936. PubMed PMC

Zubo YO, Yamburenko MV, Selivankina SY, Shakirova FM, Avalbaev AM, Kudryakova NV, Zubkova NK, Liere K, Kulaeva ON, Kusnetsov VV, et al. (2008) Cytokinin stimulates chloroplast transcription in detached barley leaves. Plant Physiol 148: 1082–1093 PubMed PMC

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