Role of transcription factors in regulating ripening, senescence and organ abscission in plants

Stewart Postharvest Review

Volumn 3, Issue 2, 2007, Pages

  Nath, Pravendra ^a   Sane, Aniruddha P ^a   Trivedi, Prabodh K ^a   Sane, Vidhu A ^a   Asif, Mehar H ^a  

^a CSIR NATIONAL BOTANICAL RESEARCH INSTITUTE   (India)

Author keywords

Abscission; Dehiscence; Ethylene signalling; Fruit ripening; Gene expression; Senescence; Transcription factors

Indexed keywords

ARABIDOPSIS; LYCOPERSICON ESCULENTUM;

EID: 34248583548     PISSN: None     EISSN: 17459656     Source Type: Journal    
DOI: 10.2212/spr.2007.2.6     Document Type: Review

References (59)

1. nd edition); 2005: pp 307-358.
2. Chen W, Provart NJ, Glazebrook J, Katagiri F, Changa H-S et al. Expression profile matrix of Arabidopsis transcription factor gene suggests their putative functions in response to environmental stress. The Plant Cell 2002:14:559-574. ** Using Arabidopsis gene chip, the authors identified 402 stress-related genes, which may encode putative TFs. About 8,300 genes were selected for analysis based on the annotation associated with probe sets on the chip. These genes included 63 AP2/EREBP genes, 121 At Myb genes, 34 bZIPgenes, 152 members of the diverse zinc-finger gene classes, 12 AtHD-ZIP and 21 IAA/AXR genes.
3. *Nath P, Trivedi PK, Sane VA and Sane AP. Role of ethylene in fruit ripening. In :Ethylene action in plants. Khan NA (ed) Springer-Verlag, Berlin Geidelberg; 2006: pp 151-185.
4. Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W and Ecker JR. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 1997: 89:1133-1144. *The group has shown that TF EIN3 and related proteins like EIL1 and 2 act downstream to ETR1 and CTR1. Overexpression of EIN3 or EIL1 in wild-type or ethylene-insensitive2 plants conferred constitutive ethylene phenotypes, indicating their sufficiency for activating the pathway in the absence of ethylene.
5. Solano R, Stepanova A, Chao Q and Ecker JR. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENERESPONSE- FACTOR1. Genes and Development 1998: 12: 3703-3714. **One of the classical papers related to the ethylene signalling cascade. The authors have shown that EIN3 and EILs comprise a family of novel sequence-specific DNA-binding proteins that regulate gene expression by binding directly to a primary ethylene response element (PERE) related to the tomato E4-element. They also identified an immediate target of EIN3, ETHYLENE RESPONSE FACTOR1 (ERF1), which contains this element in its promoter. The study demonstrated that the nuclear proteins EIN3 and ERF1 act sequentially in a cascade of transcriptional regulation initiated by ethylene gas.
6. Tieman DM, Ciardi JA, Taylor MG and Klee HJ. Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. The Plant Journal 2001: 26(1): 47-58. **The authors have identified three homologs of the Arabidopsis EIN3 gene (LeEILs) in tomato. Each of these genes complemented the ein3-1 mutation in transgenic Arabidopsis, indicating that all are involved in ethylene signal transduction. Results suggested that LeEILs are functionally redundant and positive regulators of multiple ethylene responses throughout plant development.
7. Yokotani N, Tamura S, Nakano R, Inaba A and Kubo Y. Characterization of a novel tomato EIN3-like gene (LeEIL4). Journal of Experimental Botany 2003: 54(393): 2775-2776. A novel cDNA clone encoding a putative EIN3-like protein (LeEIL4) was identified from ripening tomato and may be involved in the ethylene signal cascade. LeEIL4 transcripts accumulated in all tissues examined, with higher levels in ripening fruit.
8. Chen G, Alexander L and Grierson D. Constitutive expression of EIL-like transcription factor partially restores ripening in the ethylene-insensitive Nr tomato mutant. Journal of Experimental Botany 2004: 55(402):1491-1497 *EIL1 was overexpressed in the ethylene-insensitive non-ripening (Nr) mutant of tomato. Increased levels of LeEIL1 compensated for the normally reduced levels of LeEIL1 in the Nr mutant, and transgenic Nr plants phenotypically resembled wild-type plants. However, not all ripening genes and ethylene responses, such as seedling triple response, were restored.
9. Périn C, Gomez-Jimenez M, Hagen L, Dogimont C, Pech J-C, Latche A, Pitrat M and Lelièvre J-M. Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit. Plant Physiology 2002: 129: 300-309. Melon is a climacteric fruit, however some varieties behave as non-climacteric. The authors made crosses and genetic analysis on a population of recombinant cantaloupe Charentais X PI 161375 inbred lines in segregation for fruit abscission and ethylene production indicated that both characters are controlled by two independent loci, abscission layer (Al)-3 and Al-4. The non-climacteric phenotype in fruit tissues is attributable to ethylene insensitivity conferred by the recessive allelic forms from PI 161375.
10. Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latche A, Pech J-C and Bouzayen M. New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Letters. 2003: 550:149-154. *Four new members of the ERF family of plant-specific DNA-binding (GCC box) factors were isolated from tomato fruit (LeERF1-4). Experimental data and 3-D analysis showed that binding of the LeERFs was affected by both the variation of nucleotides surrounding the DNA cis-element sequence and the nature of critical amino acid residues within the ERF domain
11. Fei Z, Tang X, Alba RM, White JA, Ronning CM, Martin GB, Tanksley SD and Giovannoni JJ. Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. The Plant Journal 2004: 40: 47-59 *A large tomato EST dataset (152,635 total) was analysed to gain insights into differential gene expression among diverse plant tissues representing a range of developmental programs and biological responses. Tomato fruit digital expression data was specifically compared with publicly available grape EST data and resulted in identification of common TFs not previously associated with ripening.
12. Adams-Phillips L, Barry C and Giovannoni J. Signal transduction systems regulating fruit ripening. Trends in Plant Science 2004: 9:331-338. *The review describes different signal transduction systems regulating the fruit ripening process. The authors have reviewed ethylene, light signal pathways and developmental control of fruit with emphasis on identification of broadly conserved and more-specific genetic regulators of ripening in the near future.
13. Lincoln JE and Fischer RL. Diverse mechanisms for the regulation of ethylene-inducible gene expression. Molecular Genetics and Genomics 1988: 212: 71-75. *The mechanism of action of the plant hormone ethylene on expression of ethylene-inducible genes isolated from tomato has been investigated. Differential regulation of genes either on transcriptional, or both transcriptional and posttranscriptional processes have been suggested. In addition, the authors have measured gene expression as a function of ethylene concentration and have found that each gene displays a unique ethylene dose-response curve.
14. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W and Giovannoni J. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 2002: 296: 343-346. **Positional cloning of the rin locus from tomato revealed two tandem MADS-box genes (LeMADS-RIN and LeMADS-MC) whose expression patterns suggested roles in fruit ripening and sepal development, respectively. Gene repression and mutant complementation demonstrate that LeMADS-RIN regulates ripening. LeMADS-RIN demonstrates an agriculturally important function of plant MADS-box genes and provides molecular insight into non-hormonal (developmental) regulation of ripening.
15. White PJ. Recent advances in fruit development and ripening: an overview. Journal of Experimental Botany 2002 53: 1995-2000. *The author reviews significant progress made in identifying genes controlling the development of dry dehiscent fruits in the model plant species Arabidopsis thaliana. In plants with fleshy fruits, a major focus has been the dissection of biochemical and genetic regulatory cascades controlling ripening, using tomato as a model species.
16. Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ and Seymour GB. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genetics 2006: 38:948-952. **Using positional cloning and virus-induced gene silencing, it was demonstrated that an SBP-box gene controls the fruit ripening process in the Cnr mutant. Epigenetic changes in the SBP-box promoter result in alteration in expression of the SBP-box gene resulting Cnr phenotype.
17. Bogs J, Jaffe FW, Takos AM, Walker AR and Robinson SP. The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiology 2007 (in press). *The authors identify a grapevine MYB TF, VvMYBPA1, and demonstrate its involvement in controlling expression of the proanthocyanidin pathway genes leucoanthocyanidin reductase (LAR) and anthocyanidin reductase (ANR). Expression of VvMYBPA1 in grape berries correlated with PA accumulation during early berry development and in seeds.
18. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S and Allan AC. Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant Journal 2007: 49:414-427. **From studies in a diverse array of plant species, it is apparent that anthocyanin biosynthesis, an important determinant of the colour of many fruits, is controlled at the level of transcription. In this article, the authors describe an apple MYB TF, MdMYB10, that can induce anthocyanin accumulation in both heterologous and homologous systems, generating pigmented patches in transient assays in tobacco leaves and highly pigmented apple plants following stable transformation.
19. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A and Aalen RB. INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 2003: 15: 2296-2307. The authors have identified an Arabidopsis ethylene-sensitive mutant, Inflorescence deficient in abscission (ida), in which floral organs remain attached to the plant body after the shedding of mature seeds, even though a floral abscission zone develops. The IDA gene encodes a small protein with an N-terminal signal peptide, suggesting that the IDA protein is the ligand of an unknown receptor involved in the developmental control of floral abscission.
20. Fernandez DE, Heck GR, Perry SE, Patterson SE, Bleecker AB and Fang SC. The embryo MADS domain factor AGL15 acts postembryonically: inhibition of perianth senescence and abscission via constitutive expression. Plant Cell 2000: 12: 183-197. AGL15 (AGAMOUS-like 15), a member of the MADS-domain family of regulatory factors, accumulates preferentially throughout the early stages of the plant life cycle. In this study, the authors investigated the expression pattern and possible roles of postembryonic accumulation of AGL15. Using a combination of reporter genes, RNA gel blot analysis and immunochemistry, they found that the AGL15 protein accumulates transiently in the shoot apex in young Arabidopsis and Brassica seedlings and that promoter activity is associated with the shoot apex and the base of leaf petioles throughout the vegetative phase. During the reproductive phase, AGL15 accumulates transiently in floral buds.
21. Mao L, Begum D, Chuang H, Budiman M, Szymkowiak E, Irish E and Wing R. JOINTLESS is a MADS-box gene controlling flower abscission zone development. Nature 2000: 406: 910-913. The authors report the first isolation of a gene directly involved in the development of a functional plant AZ. Tomato plants with the jointless mutation fail to develop AZs on their pedicels and so abscission of flowers or fruit does not occur normally. They identify JOINTLESS as a new MADS-box gene in a distinct phylogenetic clade separate from those functioning in floral organs.
22. Schumacher K, Schmitt T, Rossberg M, Schmitz G and Theres K. The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proceedings of the National Academy of Sciences, USA 1999: 96: 290-295. In the lateral suppressor mutant of tomato, the initiation of axillary meristems is prevented, thus offering the unique opportunity to study the molecular mechanisms underlying this important function of the shoot apical meristem. The authors report on the isolation of the LATERAL SUPPRESSOR gene by positional cloning and show that the mutant phenotype is caused by a complete loss of function of a new member of the VHIID family of plant regulatory proteins.
23. Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ and Reed JW. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 2005: 132: 4563-4574. The authors have examined Arabidopsis lines carrying T-DNA insertions in AUXIN RESPONSE FACTOR1 (ARF1) and ARF2 genes. They found that ARF2 promotes transitions between multiple stages of Arabidopsis development. arf2 mutant plants exhibited delays in several processes related to plant aging, including initiation of flowering, rosette leaf senescence, floral organ abscission and silique ripening.
24. Norberg M, Holmlund M and Nilsson O. The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 2005: 132: 2203-2213. The authors have isolated and characterised the BOP1 gene together with a functionally redundant close homolog that was named BOP2. The BOP genes are members of a gene family containing ankyrin repeats and a BTB/POZ domain, suggesting a role in protein-protein interaction.
25. Pointud JC, Larsson J, Dastague B and Couderc JL. The BTB/POZ domain of the regulatory proteins BRIC A BRAC 1 (BAB1) and BRIC A BRAC 2 (BAB2) interacts with the novel Drosophila TAF(II) factor BIP2/dTAF(II) 155. Developmental Biology 2001: 237: 368-380. The authors have identified partners of the BAB1 protein by using the two-hybrid system. The characterisation of one of these proteins, called BIP2 for BAB Interacting Protein 2, is presented. BIP2 is a novel Drosophila TATA-box Protein Associated Factor (TAF(II)), also named dTAF(II)155. They show that the BTB/POZ domains of BAB1 and BAB2 are sufficient to mediate a direct interaction with BIP2/dTAF(II)155.
26. Dong XN. NPR1, all things considered. Current Opinion in Plant Biology 2004: 7: 547-552. Molecular characterisation has revealed that activation of NPR1 and certain TGA TFs occurs under the reducing conditions that follow an initial oxidative burst after the induction of defence responses. In addition to NPR1 and TGA, the single-stranded DNA-binding TF AtWhy1 and the WRKY70 TF were recently found to be involved in SA-mediated defence and SA-JA crosstalk, respectively.
27. Liu GS, Holub EB, Alonso JM, Ecker JR. and Fobert PR. An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance. Plant Journal 2005: 41: 304-318. In this paper reverse genetics was used to analyse the role of one NPR1-like gene, NPR4. The NPR4 protein shares 36% identity with NPR1 and interacts with the same spectrum of TGA TFs in yeast two-hybrid assays. Plants with T-DNA insertions in NPR4 are more susceptible to the virulent bacterial pathogen Pseudomonas syringe pv. tomato DC3000. This phenotype is complemented by expression of the wild type NPR4 coding region.
28. Tucker ML, Whitelaw CA, Lyssenko NN and Nath P. Functional analysis of regulatory elements in the gene promoter for an abscission-specific cellulase from bean and isolation, expression, and binding affinity of three TGA-type basic leucine zipper transcription factors. Plant Physiology 2002: 130: 1487-1496. **This paper identifies the cis-elements involved in hormonal and abscission-specific expression. Tandem ligation of three 18-bp BAC elements (Z-BAC), which includes the bZIP motif, to a minimal -50 35S cauliflower mosaic virus promoter enhanced expression in abscission zones (AZs) 13-fold over that of the minimal promoter alone.
29. Zhu QH, Ramm K, Shivakumar R, Dennis ES and Upadhyaya NM. The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiology 2004: 135:1514-1525. Using a two-element Ac/Ds transposon-tagging system, the authors identified a rice (Oryza sativa L. cv Nipponbare) recessive mutant, anther indehiscence1 (aid1), showing partial to complete spikelet sterility. Spikelets of the aid1 mutant could be classified into three types based on the viability of pollen grains and the extent of anther dehiscence.
30. Steiner-Lange S, Unte US, Eckstein L, Yang C, Wilson ZA, Schmelzer E, Dekker K and Saedler H. Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant Journal 2003: 34:519-528. A male sterile mutant with a defect in anther dehiscence was identified in an Arabidopsis thaliana population mutagenised with the Zea mays transposon En-1/Spm. Mutants produce viable pollen that can fertilise when released mechanically from the anthers. Mutant stamens are of normal size and shape, but lack cell wall fortifications in the endothecial cell layer of the anther, which are required for the dehiscence process. The mutant phenotype was shown to be caused by a transposon insertion in AtMYB26, disrupting the putative DNA-binding domain of this R2R3-type MYB TF.
31. Pinyopich A, Ditta GS, Savidge B, Liljegren, SJ, Baumann E, Wisman E, Yanofsky MF. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 2003: 424: 85-88. The authors show that the SHP genes are responsible for AG-independent carpel development. They also show that the STK gene is required for normal development of the funiculus, an umbilical-cord-like structure that connects the developing seed to the fruit, and for dispersal of the seeds when the fruit matures. They further show that all four members of the AG clade are required for specifying the identity of ovules, the landmark invention during the course of vascular plant evolution that enabled seed plants to become the most successful group of land plants.
32. Rajani S and Sundaresan V. The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Current Biology 2001: 11: 1914-1922. The authors describe a novel mutation in Arabidopsis called alcatraz (alc), which prevents dehiscence of fruit by specifically blocking the separation of the valve cells from the replum. The ALC gene is shown to encode a protein related to the myc/bHLH family of TFs and is expressed in the valve margins of the silique, which is the site of cell separation during dehiscence.
33. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL and Yanofsky MF. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 2000: 404: 766-770. Here the authors show that the closely related SHATTERPROOF (SHP1) and SHATTERPROOF2 (SHP2) MADS-box genes are required for fruit dehiscence in Arabidopsis. Moreover, SHP1 and SHP2 are functionally redundant, as neither single mutant displays a novel phenotype. Their studies of shp1shp2 fruit, and of plants constitutively expressing SHP1 and SHP2, show that these two genes control dehiscence zone differentiation and promote the lignification of adjacent cells.
34. Liljegren SJ, Roeder AH, Kempin SA, Gremski K, Ostergaard L, Guimil S, Reyes DK and Yanofsky MF. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 2004: 116: 843-853. *This paper characterises the role of IND, SHP, ALC and FUL during valve margin differentiation. It shows that FUL is found to promote valve differentiation primarily by restricting the expression of IND, SHP and ALC at the valve margin.
35. Lewis MW, Leslie ME and Liljegren SJ. Plant separation: 50 ways to leave your mother. Current Opinion in Biology 2006: 9: 59-65. **This review beautifully illustrates the transcriptional network involved in different plant separation processes.
36. Roeder AH, Ferrándiz C and Yanofsky MF. The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Current Biology 2003: 13: 1630-1635. Here the authors identify a gene called REPLUMLESS that is required for replum development. REPLUMLESS encodes a homeodomain protein that prevents replum cells from adopting a valve margin cell fate by negatively regulating expression of the SHATTERPROOF genes. Both REPLUMLESS and FRUITFULL are required to limit SHATTERPROOF expression to row stripe of cells so that the valve margin differentiates precisely at the valve/replum boundary.
37. Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T and Yano M. An SNP caused loss of seed shattering during rice domestication. Science 2006: 312: 1392-1396. **The authors revealed that the qSH1 gene, a major quantitative trait locus of seed shattering in rice, encodes a BEL1-type homeobox gene and demonstrated that a single-nucleotide polymorphism (SNP) 12kb 'upstream' in the promoter of the qSH1 gene caused loss of seed shattering owing to the absence of abscission layer formation. Haplotype analysis and association analysis in various rice collections revealed that the SNP was highly associated with shattering among japonica subspecies of rice, implying that it was a target of artificial selection during rice domestication.
38. Li C, Zhou A and Sang T. Rice domestication by reducing shattering. Science 2006: 311: 1936-1939. **The authors show that human selection of an amino acid substitution in the predicted DNA binding domain encoded by SH4 gene of unknown function was primarily responsible for the reduction of grain shattering in rice domestication. The substitution undermined the gene function necessary for the normal development of an abscission layer that controls the separation of a grain from the pedicel.
39. Rubinstein B. Regulation of cell death in flower petals. Plant Molecular Biology 2000: 44: 303-318. This comprehensive review provides a detailed analysis of changes taking place during the cell death program in petals.
40. Rogers HJ. Programmed cell death in floral organs: How and why do flowers die? Annals of Botany 2006: 97: 309-315. *This review on programmed cell death (PCD) in floral organs discusses the timing of PCD, possible mechanisms and compares cell death in other organs.
41. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S and Page T. and Pink D. (2003) The molecular analysis of leaf senescence - a genomics approach. Plant Biotechnology Journal 2003: 1: 3-22. In this review, the mechanisms by which plants control senescence and the processes that are involved have been described.
42. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin J-F, Wu S-H, Swidzinski J, Ishizaki K and Leaver CJ. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant Journal 2005: 42: 567-585. **The authors performed a comprehensive gene expression analysis during developmental, dark-induced senescence, sugar starvation-induced senescence and also compared gene expression in SA, JA and ethylene mutants. They showed that each type of senescence was associated with expression of genes common to all, as well as several genes unique to each form of senescence.
43. Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MFO, Yariv I, Dor C and Bassani M. Large-scale identification of leaf senescence-associated genes. Plant Journal 2003: 36: 629-642. *Using suppression subtractive hybridisation, the authors isolated approximately 800 cDNA clones representing senescence-associated genes (SAGs) expressed in senescing Arabidopsis leaves. Expression of some of the novel SAGs, in response to age, leaf detachment, darkness, and ethylene and cytokinin treatment, was compared.
44. Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Bjorkbacka H, Birve SJ, Karlsson J, Gardestrom P, Gustafsson P, Lundeberg J and Jansson S. Gene expression in autumn leaves. Plant Physiology 2003:131: 430-442. The authors provided the first senescence-associated transcriptome study of a tree species. They made two cDNA libraries of Populus leaves of different stages and identified many homologs of senescence-associated genes.
45. Guo Y, Cai Z and Gan S. Transcriptome of Arabidopsis leaf senescence. Plant Cell Environment 2004: 27: 521-549. Leaf senescence cDNA library of Arabidopsis was constructed and EST data analysis suggested that there are 134 genes encoding TFs and 182 genes whose products are components of signal transduction pathways.
46. Lin JF and Wu SH. Molecular events in senescing Arabidopsis leaves. Plant Journal 2004: 39: 612-628. Using a microarray system, the authors established association of GRAS, WRKY, NAC, bZIP and C2H2 TF families in leaf senescence.
47. Gregersen PL and Holm PB. Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotechnology Journal 2007: 5: 192-206. The senescence process in wheat flag leaves was investigated over a time course from ear emergence until 50% yellowing of harvested leaf samples by cDNA microarray. Several TFs of the NAC family and WRKY family were found to be expressed during senescence.
48. Uauy C, Distelfeld A, Fahima T, Blechl A and Dubcovsky J. A NAC gene regulating senescence improves grain protein, zinc and iron content in wheat. Science 2006: 314: 1298-1301. **This paper describes the work on positional cloning of NAM-B1 gene from wheat, which encodes NAC TF. It provides a direct link between the regulation of flag leaf senescence and protein and nutrient remobilisation from leaves to the grain.
49. Eulgem T, Rushton PJ, Robatzek S and Somssich IE. The WRKY superfamily of plant transcription factors. Trends in Plant Science 2000: 5: 199-206. **This review provides detailed information about the WRKY family of proteins. Family members appear to be involved in the regulation of various physiological programs that are unique to plants, including pathogen defence, senescence and trichome development.
50. Robatzek S and Somssich IE. Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes and Development 2002: 16:1139-1149. *The authors characterised the WRKY6 gene and identified its role as a repressor of its own promoter and an activator of other genes such as SIRK and SARK.
51. Hinderhofer K and Zentgraf U. Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 2001: 213: 469-473. Using SSH, authors analysed the differential expression of WRKY53 during leaf senescence in Arabidopsis. Their study indicated that WRKY53 is expressed at a very early time point of leaf senescence and might therefore play a regulatory role in the early events of senescence.
52. Miao Y, Laun T, Zimmermann P and Zentgraf U. Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Molecular Biology 2004: 55: 853-867. The authors used pull-down assay to identify target genes of Arabidopsis WRKY53 TF using genomic DNA and Recombinant WRKY53 protein. Several WRKY proteins were identified as targets of the WRKY53 protein indicating that it activates a signalling network regulating senescence-related gene expression.
53. Guo Y and Gan S. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant Journal 2006: 46: 601-612. *This group reported the functional analysis of AtNAP, a gene encoding a NAC family TF. Expression of this gene was closely associated with the senescence process of Arabidopsis rosette leaves. Leaf senescence in two T-DNA insertion lines of this gene was significantly delayed.
54. Kong Z, Li M, Yang W, Xu W and Xue Y. A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiology 2006: 141: 1376-1388. **A novel repressor of leaf senescence was identified in rice that delayed senescence by regulating the jasmonate pathway.
55. Fang S-C and Fernandez DE. Effect of regulated overexpression of the MADS domain factor AGL15 on flower senescence and fruit maturation. Plant Physiology 2002: 130: 78-89. Using molecular and physiological markers, the authors showed that constitutive overexpression of AGL15 in Arabidopsis led to delay and down-regulation of senescence programs in perianth organs and developing fruits, and altered the process of seed desiccation.
56. van Doorn WG, Balk PA, van Houwelingen AM, Hoeberichts FA, Hall RD, Vorst O, van der Schoot C and van Wordragen MF. Gene expression during anthesis and senescence in Iris flowers. Plant Molecular Biology 2003: 53: 845-863. The authors investigated changes in gene expression in Iris flowers by microarray technology and identified several floral senescence-associated positive regulators of transcription and translation including a MADS- domain factor.
57. Shibuya K, Barry KG, Ciardi JA, Loucas HM, Underwood BA, Nourizadeh S,. Ecker JR, Klee HJ and Clark DG. The central role of PhEIN2 in ethylene responses throughout plant development in petunia. Plant Physiology 2004:136: 2900-2912. The authors isolated a petunia homolog of the Arabidopsis EIN2 gene (PhEIN2). They showed that expression of PhEIN2 mRNA is spatially and temporally regulated in petunia during plant development. It was also demonstrated that PhEIN2 mediates ethylene signals in a wide range of physiological processes.
58. Waki K, Shibuya K, Yoshioka T, Hashiba T and Satoh S. Cloning of cDNA encoding EIN3 likeprotein (Dc-EIL1) and decrease of its mRNA level during senescence in carnation flower tissues. Journal of Experimental Botany 2001: 52: 377-379. *Gene encoding putative EIN3 like protein (DC-EIL) was identified from carnation. The transcript was decreased during natural petal and ethylene and ABA-induced senescence.
59. Manavella PA, Arce AL, Dezar CA, Bitton F, Renou J-P, Crespi M and Chan RL. Cross-talk between ethylene and drought signaling pathways is mediated by the sunflower Hahb-4 transcription factor. The Plant Journal 2006: 48: 125-137. *The authors show through over-expression of sunflower Hahb-4 in Arabidopsis that it interacts with the ethylene signalling pathway as well as with the drought signalling pathways and affects the expression of ethylene biosynthetic and signal transduction genes.