Regulation of Leaf Senescence and Crop Genetic Improvement

Journal of Integrative Plant Biology

Volumn 54, Issue 12, 2012, Pages 936-952

  Wu, Xiao Yuan ^a   Kuai, Ben Ke ^b   Jia, Ji Zeng ^c   Jing, Hai Chun ^a  

^a INSTITUTE OF BOTANY   (China)

^b FUDAN UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Crop ideotypes; Leaf Senescence; Nutrient remobilisation; Photosynthesis and photoassimilates; Senescence associated genes

Indexed keywords

CROP PRODUCTION; GENETIC ENGINEERING; LEAF; PHOTOSYNTHESIS; SENESCENCE;

BIOMASS; CROP; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; REVIEW;

BIOMASS; CROPS, AGRICULTURAL; PHOTOSYNTHESIS; PLANT LEAVES;

EID: 84870863293     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12005     Document Type: Review

References (157)

1. Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol. 152, 656-669.
2. Araujo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, Leaver CJ, Fernie AR (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22, 1549-1563.
3. Ay N, Irmler K, Fischer A, Uhlemann R, Reuter G, Humbeck K (2009) Epigenetic programming via histone methylation at WRKY53 controls leaf senescence in Arabidopsis thaliana. Plant J. 58, 333-346.
4. Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Kohler B, Mueller-Roeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 62, 250-264.
5. Barzilai N, Guarente L, Kirkwood TB, Partridge L, Rando TA, Slagboom PE (2012) The place of genetics in ageing research. Nat. Rev. Genet. 13, 589-594.
6. Bassham DC (2007) Plant autophagy-more than a starvation response. Curr. Opin. Plant Biol. 10, 587-593.
7. Besseau S, Li J, Palva ET (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot doi: 10.1093/jxb/err450
8. Bleecker AB (1998) The evolutionary basis of leaf senescence: Method to the madness Curr. Opin. Plant Biol. 1, 73-78.
9. Bleecker AB, Patterson SE (1997) Last exit: Senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9, 1169-1179.
10. Bogard M, Jourdan M, Allard V, Martre P, Perretant MR, Ravel C, Heumez E, Orford S, Snape J, Griffiths S, Gaju O, Foulkes J, Le Gouis J (2011) Anthesis date mainly explained correlations between post-anthesis leaf senescence, grain yield, and grain protein concentration in a winter wheat population segregating for flowering time QTLs. J. Exp. Bot. 62, 3621-3636.
11. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang C, Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23, 873-894.
12. Brevis JC, Morris CF, Manthey F, Dubcovsky J (2010) Effect of the grain protein content locus Gpc-B1 on bread and pasta quality. J. Cereal Sci. 51, 357-365.
13. Brychkova G, Alikulov Z, Fluhr R, Sagi M (2008) A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. Plant J. 54, 496-509.
14. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence - A genomics approach. Plant Biotechnol. J. 1, 3-22.
15. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (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.
16. 4 plants as biofuel feedstocks: Optimising biomass production and feedstock quality from a lignocellulosic perspective. J. Integr. Plant Biol. 53, 120-135.
17. Calvino M, Messing J (2012) Sweet sorghum as a model system for bioenergy crops. Curr. Opin. Plant Biol. 23, 323-329.
18. Canas RA, Quillere I, Lea PJ, Hirel B (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotechnol. J. 8, 966-978.
19. Castillo MC, Leon J (2008) Expression of the beta-oxidation gene 3-ketoacyl-CoA thiolase 2 (KAT2) is required for the timely onset of natural and dark-induced leaf senescence in Arabidopsis. J. Exp. Bot 59, 2171-2179.
20. Causier B, Kieffer M, Davies B (2002) Plant biology: MADS-Box genes reach maturity. Science 296, 275-276.
21. Chardon F, Barthelemy J, Daniel-Vedele F, Masclaux-Daubresse C (2010) Natural variation of nitrate uptake and nitrogen use efficiency in Arabidopsis thaliana cultivated with limiting and ample nitrogen supply. J. Exp. Bot 61, 2293-2302.
22. Chen GH, Chan YL, Liu CP, Wang LC (2012a) Ethylene response pathway is essential for ARABIDOPSIS A-FIFTEEN function in floral induction and leaf senescence. Plant Signal. Behav. 7, 457-460.
23. Chen GH, Liu CP, Chen SC, Wang LC (2012b) Role of ARABIDOPSIS A-FIFTEEN in regulating leaf senescence involves response to reactive oxygen species and is dependent on ETHYLENE INSENSITIVE2. J. Exp. Bot. 63, 275-292.
24. Davies WJ, Zhang J, Yang J, Dodd IC (2011) Novel crop science to improve yield and resource use efficiency in water-limited agriculture. J. Agr. Sci. 149, 123-131.
25. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277, 33105-33114.
26. Donnison IS, Gay AP, Thomas H, Edwards KJ, Edwards D, James CL, Thomas AM, Ougham HJ (2007) Modification of nitrogen remobilization, grain fill and leaf senescence in maize (Zea mays) by transposon insertional mutagenesis in a protease gene. New Phytol. 173, 481-494.
27. Feller U, Anders I, Mae T (2008) Rubiscolytics: Fate of Rubisco after its enzymatic function in a cell is terminated. J. Exp. Bot. 59, 1615-1624.
28. Fleming AJ (2006) Leaf initiation: The integration of growth and cell division. Plant Mol. Biol. 60, 905-914.
29. Frelet-Barrand A, Kolukisaoglu HU, Plaza S, Ruffer M, Azevedo L, Hortensteiner S, Marinova K, Weder B, Schulz B, Klein M (2008) Comparative mutant analysis of Arabidopsis ABCC-type ABC transporters: AtMRP2 contributes to detoxification, vacuolar organic anion transport and chlorophyll degradation. Plant Cell Physiol. 49, 557-569.
30. Gan S (2012) Regulation of senescence by plant growth substances. Xu ZH, Xue HW, eds. Molecular Mechanisms of Plant Hormone Actions Shanghai Science and Technology Press. pp. 405-424.
31. Gan SS, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270, 1986-1988.
32. Gan SS, Amasino RM (1997) Making sense of senescence - Molecular genetic regulation and manipulation of leaf senescence. Plant Physiol. 113, 313-319.
33. Gaufichon L, Masclaux-Daubresse C, Tcherkez G, Reisdorf-Cren M, Sakakibara Y, Hase T, Clement G, Avice JC, Grandjean O, Marmagne A, Boutet-Mercey S, Azzopardi M, Soulay F, Suzuki A (2012) Arabidopsis thaliana ASN2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth. Plant Cell Environ. doi: 10.1111/j.1365-3040.2012.02576.x.
34. Gebbing T, Schnyder H (1999) Pre-anthesis reserve utilization for protein and carbohydrate synthesis in grains of wheat. Plant Physiol 121, 871-878.
35. Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MF, Yariv I, Dor C, Bassani M (2003) Large-scale identification of leaf senescence-associated genes. Plant J. 36, 629-642.
36. Gong YH, Zhang J, Gao JF, Lu JY, Wang JR (2005) Slow export of photoassimilate from stay-green leaves during late grain-filling stage in hybrid winter wheat (Triticum aestivum L.). J. Agron. Crop Sci. 191, 292-299.
37. Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol. 10, 37-49.
38. Guiboileau A, Yoshimoto K, Soulay F, Bataille MP, Avice JC, Masclaux-Daubresse C (2012) Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol. 194, 732-740.
39. Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17, 3436-3450.
40. Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 27, 521-549.
41. Guo Y, Gan SS (2012) Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ. 35, 644-655.
42. Guo YF, Gan SS (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601-612.
43. Guo YF, Gan SS (2011) AtMYB2 regulates whole plant senescence by inhibiting cytokinin-mediated branching at late stages of development in Arabidopsis. Plant Physiol. 156, 1612-1619.
44. Gurr SJ, Rushton PJ (2005) Engineering plants with increased disease resistance: How are we going to express it Trends Biotechnol 23, 283-290.
45. Hafsi M, Mechmeche W, Bouamama L, Djekoune A, Zaharieva M, Monneveux P (2000) Flag leaf senescence, as evaluated by numerical image analysis, and its relationship with yield under drought in durum wheat. J. Agron. Crop Sci. 185, 275-280.
46. Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (2002) Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129, 1181-1193.
47. Harris K, Subudhi PK, Borrell A, Jordan D, Rosenow D, Nguyen H, Klein P, Klein R, Mullet J (2007) Sorghum stay-green QTL individually reduce post-flowering drought-induced leaf senescence. J. Exp. Bot. 58, 327-338.
48. Hensel LL, Bleecker AB (1992) Arabidopsis as a model system for analysis of leaf senescence and inflorescence-meristem longevity. Amasine RM, ed. Proceedings of the Twenty-First Steenbock Symposium: Cellular Communication in Plants Plenum Press, New York pp.123-130.
49. Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J. Plant Physiol. 158, 1317-1323.
50. Hirel B, Bertin P, Quillere I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol. 125, 1258-1270.
51. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: Towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58, 2369-2387.
52. Hörtensteiner S. (2012) Update on the biochemistry of chlorophyll breakdown. Plant Mol. Biol. DOI 10.1007/s11103-012-9940-z
53. Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J. Exp. Bot. 53, 927-937.
54. Hortensteiner S, Krautler B (2011) Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 1807, 977-988.
55. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T (2008) Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol. 148, 142-155.
56. 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.
57. Jackson SD (2009) Plant responses to photoperiod. New Phytol. 181, 517-531.
58. Jaggard KW, Qi A, Ober ES (2010) Possible changes to arable crop yields by 2050. Philos. Trans. R. Soc. London, Ser. B 365, 2835-2851.
59. Jiao BB, Wang JJ, Zhu XD, Zeng LJ, Li Q, He ZH (2012) A novel protein RLS1 with NB-ARM domains is involved in chloroplast degradation during leaf senescence in rice. Mol. Plant 5, 205-217.
60. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541-544.
61. Jin Y, Ni DA, Ruan YL (2009) Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21, 2072-2089.
62. Jing HC, Anderson L, Sturre MJG, Hille J, Dijkwel PP (2007) Arabidopsis CPR5 is a senescence-regulatory gene with pleiotropic functions as predicted by the evolutionary theory of senescence. J. Exp. Bot 58, 3885-3894.
63. Jing HC, Hebeler R, Oeljeklaus S, Sitek B, Stuehler K, Meyer HE, Sturre MJG, Hille J, Warscheid B, Dijkwel PP (2008) Early leaf senescence is associated with an altered cellular redox balance in Arabidopsis cpr5/old1 mutants. Plant Biol. 10, 85-98.
64. Jing HC, Hille J, Dijkwel RR (2003) Ageing in plants: Conserved strategies and novel pathways. Plant Biol. 5, 455-464.
65. Jing HC, Schippers JHM, Hille J, Dijkwei PP (2005) Ethylene-induced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J. Exp. Bot 56, 2915-2923.
66. Jing HC, Sturre MJG, Hille J, Dijkwel PP (2002) Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J. 32, 51-63.
67. Kato Y, Sakamoto W (2010) New insights into the types and function of proteases in plastids. Int. Rev. Cell Mol. Biol. 280, 185-218.
68. Kenyon CJ (2010) The genetics of ageing. Nature 464, 504-512.
69. Kim CY, Bove J, Assmann SM (2008) Overexpression of wound-responsive RNA-binding proteins induces leaf senescence and hypersensitive-like cell death. New Phytol. 180, 57-70.
70. Kim JH, Chung KM, Woo HR (2011a) Three positive regulators of leaf senescence in Arabidopsis, ORE1, ORE3 and ORE9, play roles in crosstalk among multiple hormone-mediated senescence pathways. Genes Genom. 33, 373-381.
71. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323, 1053-1057.
72. Kim JI, Murphy AS, Baek D, Lee SW, Yun DJ, Bressan RA, Narasimhan ML (2011b) YUCCA6 over-expression demonstrates auxin function in delaying leaf senescence in Arabidopsis thaliana. J. Exp. Bot 62, 3981-3992.
73. Klee HJ (2010) Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytol. 187, 44-56.
74. Lanner RM (2002) Why do trees live so long Ageing Res. Rev. 1, 653-671.
75. Lanner RM, Connor KF (2001) Does bristlecone pine senesce Exp. Gerontol. 36, 675-685.
76. Lee IC, Hong SW, Whang SS, Lim PO, Nam HG, Koo JC (2011) Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis Leaves. Plant Cell Physiol. 52, 651-662.
77. Lee RH, Hsu JH, Huang HJ, Lo SF, Chen SCG (2009) Alkaline alpha-galactosidase degrades thylakoid membranes in the chloroplast during leaf senescence in rice. New Phytol. 184, 596-606.
78. Lee S, Seo PJ, Lee HJ, Park CM (2012a) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J. 70, 831-844.
79. Lee SJ, Jung HJ, Kang H, Kim SY (2012b) Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant Cell Physiol. 53, 673-686.
80. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu. Rev. Plant Biol. 58, 115-136.
81. Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, Woo HR, Nam HG (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J. Exp. Bot. 61, 1419-1430.
82. Lippold F, vom Dorp K, Abraham M, Holzl G, Wewer V, Yilmaz JL, Lager I, Montandon C, Besagni C, Kessler F, Stymne S, Dormann P (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell 24, 2001-2014.
83. Lobell DB, Sibley A, Ortiz-Monasterio JI (2012) Extreme heat effects on wheat senescence in India. Nat. Clim. Change 2, 186-189.
84. Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields Plant Cell Environ. 29, 315-330.
85. Lossl AG, Waheed MT (2011) Chloroplast-derived vaccines against human diseases: Achievements, challenges and scopes. Plant Biotechnol. J. 9, 527-539.
86. Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, Terce-Laforgue T, Quillere I, Coque M, Gallais A, Gonzalez-Moro MB, Bethencourt L, Habash DZ, Lea PJ, Charcosset A, Perez P, Murigneux A, Sakakibara H, Edwards KJ, Hirel B (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18, 3252-3274.
87. Martinez DE, Costa ML, Gomez FM, Otegui MS, Guiamet JJ (2008) 'Senescence-associated vacuoles' are involved in the degradation of chloroplast proteins in tobacco leaves. Plant J. 56, 196-206.
88. Masclaux-Daubresse C, Chardon F (2011) Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. J. Exp. Bot. 62, 2131-2142.
89. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Ann. Bot. 105, 1141-1157.
90. Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M (2008) Leaf nitrogen remobilisation for plant development and grain filling. Plant Biol. (Stuttg). 10 (Suppl) 1, 23-36.
91. Mi GH, Tang L, Zhang F, Zhang JH (2002) Carbohydrate storage and utilization during grain filling as regulated by nitrogen application in two wheat cultivars. J. Plant Nutr. 25, 213-229.
92. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol. Biol. 55, 853-867.
93. Miao Y, Laun TM, Smykowski A, Zentgraf U (2007) Arabidopsis MEKK1 can take a short cut: It can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol. Biol. 65, 63-76.
94. Miao Y, Smykowski A, Zentgraf U (2008) A novel upstream regulator of WRKY53 transcription during leaf senescence in Arabidopsis thaliana. Plant Biol. (Stuttg). 10 (Suppl) 1, 110-120.
95. Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19, 819-830.
96. Miao Y, Zentgraf U (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J. 63, 179-188.
97. Navabpour S, Morris K, Allen R, Harrison E, S AH-M, Buchanan-Wollaston V (2003) Expression of senescence-enhanced genes in response to oxidative stress. J. Exp. Bot. 54, 2285-2292.
98. Nooden LD, Penney JP (2001) Correlative controls of senescence and plant death in Arabidopsis thaliana (Brassicaceae). J. Exp. Bot. 52, 2151-2159.
99. 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.
100. Ono K, Nishi Y, Watanabe A, Terashima I (2001) Possible mechanisms of adaptive leaf senescence. Plant Biol. 3, 234-243.
101. Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Andrew Staehelin L, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 41, 831-844.
102. Ougham H, Hortensteiner S, Armstead I, Donnison I, King I, Thomas H, Mur L (2008) The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence. Plant Biol. 10, 4-14.
103. Pan HR, Liu SM, Tang DZ (2012) HPR1, a component of the THO/TREX complex, plays an important role in disease resistance and senescence in Arabidopsis. Plant J. 69, 831-843.
104. Parry MAJ, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu XG, Price GD, Condon AG, Furbank RT (2011) Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J. Exp. Bot. 62, 453-467.
105. Patel S, Dinesh-Kumar SP (2008) Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4, 20-27.
106. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400, 256-261.
107. Qiao Y, Jiang W, Lee J, Park B, Choi MS, Piao R, Woo MO, Roh JH, Han LZ, Paek NC, Seo HS, Koh HJ (2010) SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit mu 1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytol. 185, 258-274.
108. Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci. 5, 278-282.
109. Quirino BF, Reiter WD, Amasino RD (2001) One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol. Biol. 46, 447-457.
110. Richards RA (2000) Selectable traits to increase crop photosynthesis and yield of grain crops. J. Exp. Bot. 51, 447-458.
111. Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA 104, 19631-19636.
112. Robson P, Mos M, Clifton-Brown J, Donnison I (2012) Phenotypic variation in senescence in miscanthus: Towards optimising biomass quality and quantity. Bioenerg. Res. 5, 95-105.
113. Rolletschek H, Hosein F, Miranda M, Heim U, Gotz KP, Schlereth A, Borisjuk L, Saalbach I, Wobus U, Weber H (2005) Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and pea increases storage proteins. Plant Physiol. 137, 1236-1249.
114. Rooney WL, Aydin S (1999) Genetic control of a photoperiod-sensitive response in Sorghum bicolor (L.) Moench. Crop Sci. 39, 397-400.
115. Sakuraba Y, Balazadeh S, Tanaka R, Mueller-Roeber B, Tanaka A (2012a) Overproduction of Chl b retards senescence through transcriptional reprogramming in Arabidopsis. Plant Cell Physiol. 53, 505-517.
116. Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andres CB, Kessler F, Hortensteiner S, Paek NC (2012b) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during Leaf Senescence in Arabidopsis. Plant Cell 24, 507-518.
117. Sanders A, Collier R, Trethewy A, Gould G, Sieker R, Tegeder M (2009) AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J. 59, 540-552.
118. Sarvepalli K, Nath U (2011) Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J. 67, 595-607.
119. Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M (2009) Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J. 57, 120-131.
120. Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hortensteiner S (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21, 767-785.
121. Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol. 6, e230.
122. Shirzadian-Khorramabad R, Jing HC, Everts GE, Schippers JHM, Hille J, Dijkwel PP (2010) A mutation in the cytosolic O-acetylserine (thiol) lyase induces a genome-dependent early leaf death phenotype in Arabidopsis. BMC Plant Biol. 10.
123. Smykowski A, Zimmermann P, Zentgraf U (2010) G-Box binding factor1 reduces CATALASE2 expression and regulates the onset of leaf senescence in Arabidopsis. Plant Physiol. 153, 1321-1331.
124. 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.
125. Taylor L, Nunes-Nesi A, Parsley K, Leiss A, Leach G, Coates S, Wingler A, Fernie AR, Hibberd JM (2010) Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J. 62, 641-652.
126. Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327, 818-822.
127. Thomas H (2002) Ageing in plants. Mech. Ageing Dev. 123, 747-753.
128. Thomas H, Howarth CJ (2000) Five ways to stay green. J. Exp. Bot. 51, 329-337.
129. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298-1301.
130. Ülker B, Shahid Mukhtar M, Somssich I (2007) The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226, 125-137.
131. 2+-dependent physiological responses and act in a synergistic manner. J. Exp. Bot. 62, 3671-3682.
132. Vainonen JP, Jaspers P, Wrzaczek M, Lamminmaki A, Reddy RA, Vaahtera L, Brosche M, Kangasjarvi J (2012) RCD1-DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. Biochem. J. 442, 573-581.
133. Valente MAS, Faria JAQA, Soares-Ramos JRL, Reis PAB, Pinheiro GL, Piovesan ND, Morais AT, Menezes CC, Cano MAO, Fietto LG, Loureiro ME, Aragao FJL, Fontes EPB (2009) The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco. J. Exp. Bot. 60, 533-546.
134. Van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 141, 776-792.
135. von Saint Paul V, Zhang W, Kanawati B, Geist B, Faus-Kessler T, Schmitt-Kopplin P, Schaffner AR (2011) The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23, 4124-4145.
136. 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.
137. Waditee-Sirisattha R, Shibato J, Rakwal R, Sirisattha S, Hattori A, Nakano T, Takabe T, Tsujimoto M (2011) The Arabidopsis aminopeptidase LAP2 regulates plant growth, leaf longevity and stress response. New Phytol. 191, 958-969.
138. Walter A, Silk WK, Schurr U (2009) Environmental effects on spatial and temporal patterns of leaf and root growth. Ann. Rev. Plant Biol. 60, 279-304.
139. Warner N, Breeze E, Harrison E, Buchanan-Wollaston V (2007) Unravelling the roles of two senescence-enhanced MYB transcription factors. Comp. Biochem. Phys. A 146, S268-S268.
140. Waters BM, Uauy C, Dubcovsky J, Grusak MA (2009) Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J. Exp. Bot. 60, 4263-4274.
141. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13, 1779-1790.
142. Woo HR, Goh CH, Park JH, de la Serve BT, Kim JH, Park YI, Nam HG (2002) Extended leaf longevity in the ore4-1 mutant of Arabidopsis with a reduced expression of a plastid ribosomal protein gene. Plant J. 31, 331-340.
143. Woo HR, Kim JH, Kim J, Kim J, Lee U, Song IJ, Kim JH, Lee HY, Nam HG, Lim PO (2010) The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis. J. Exp. Bot. 61, 3947-3957.
144. Wu AH, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munne-Bosch S, Antonio C, Tohge T, Fernie AR, Kaufmann K, Xue GP, Mueller-Roeber B, Balazadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24, 482-506.
145. Xiao S, Chye ML (2010) The Arabidopsis thaliana ACBP3 regulates leaf senescence by modulating phospholipid metabolism and ATG8 stability. Autophagy 6, 802-804.
146. Xiao S, Gao W, Chen QF, Chan SW, Zheng SX, Ma JY, Wang MF, Welti R, Chye ML (2010) Overexpression of Arabidopsis Acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell 22, 1463-1482.
147. Xu F, Meng T, Li P, Yu Y, Cui Y, Wang Y, Gong Q, Wang NN (2011) A soybean dual-specificity kinase, GmSARK, and its Arabidopsis homolog, AtSARK, regulate leaf senescence through synergistic actions of auxin and ethylene. Plant Physiol. 157, 2131-2153.
148. Yamada K, Matsushima R, Nishimura M, Hara-Nishimura I (2001) A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing Arabidopsis leaves. Plant Physiol. 127, 1626-1634.
149. Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc. Natl. Acad. Sci. USA 101, 7833-7838.
150. Yang JC, Zhang JH (2006) Grain filling of cereals under soil drying. New Phytol. 169, 223-236.
151. Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23, 2155-2168.
152. Zentgraf U, Laun T, Miao Y (2010) The complex regulation of WRKY53 during leaf senescence of Arabidopsis thaliana. Eur. J. Cell Biol. 89, 133-137.
153. Zhang KW, Gan SS (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol. 158, 961-969.
154. Zhang KW, Xia XY, Zhang YY, Gan SS (2012) An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J. 69, 667-678.
155. Zhang X, Ju HW, Chung MS, Huang P, Ahn SJ, Kim CS (2011) The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol. 52, 138-148.
156. Zhou CJ, Cai ZH, Guo YF, Gan SS (2009) An Arabidopsis Mitogen-Activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol. 150, 167-177.
157. Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Ann. Rev. Plant Biol. 61, 235-261.