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Flower senescence-strategies and some associated events.

Introduction

Senescence comprises those processes that follow physiological maturity which lead to the event of death of a whole plant, organ or tissue at macroscopic level. At microscopic level the process, however is continuous, since there exists always a turnover of cell organelles at one or other places of the whole body (Voleti et al., 2000; van Doom & Woltering, 2008; Yamada et al., 2009). Senescence is an integral part of the normal developmental cycle of plants and can be viewed on a cell, tissue, organ or organization level. It is the final event in the life of many plant tissues and is highly regulated process that involves structural, biochemical and molecular changes that in many cases bear the hallmarks of programmed cell death, PCD (Makrides & Goldthwaite, 1981; Noh & Amasino, 1999; Buchanan-wollaston & Morris, 2000; Rubinstein, 2000; Xu & Hanson, 2000; Mahagamasekera & David, 2001; Leverentz et al., 2002; Wagstaff et al., 2003; Jones et al., 2005; Rogers, 2006; Xu et al., 2006; Hoeberichts et al., 2007; Ichimura et al., 2009; Lerslerwong et al., 2009; Yamada et al., 2009). It is a dynamic and closely regulated developmental process which involves highly coordinated changes in gene expression and requires active gene transcription and protein translation (Hensel et al., 1993; Yamada et al., 2003; Hoeberichts et al., 2005; Jones, 2008; Chapin & Jones, 2007, 2009). It is largely an oxidative process involving a general degradation of cellular structures and the mobilization of the products of degradation to other parts of the plants or organs (Nichols & Ho, 1975; Feller & Keist, 1986; Bieleski, 1995; Fischer et al., 1998; van Doom & Woltering, 2008). Senescence in the modular sense is generally considered a beneficial process which increases the individual fitness by allowing a plant to get rid of the old redundant structures or as prelude to the onset of harsh environments (e.g. leaf fall) but in the evolutionary sense, senescence is a deleterious phenomenon which decreases the fitness of the individual (Roach, 1993).

The term senescence and PCD have led to some confusion. The term PCD is now applied to death of cells, both in culture and in the intact organism and is used as a synonym for senescence at the cellular level. Plant scientists, applied the term PCD mainly to the death of cells and tissues and the term 'senescence' to the death of individuals and organs, as also in conjuction with death of tissues (e.g. endosperm senescence) or sometimes individual cells (Pollen tapetal cells) (Delorme et al., 2000). Senescence resembles animal cell death called apoptosis in many features but the characteristic signs of apoptosis have not been convincingly demonstrated in plants (Nooden & Guiamet, 1996; Nooden et al., 1997; Yamada et al., 2003; Hoeberichts et al., 2005; Reape & Mc Cabe, 2008; Yamada et al., 2009). Literature on senescence, postharvest physiology and technology has been reviewed by various authors (Halevy & Mayak, 1979, 1981; Nooden & Leopold, 1988; Reid, 1989; Salunkhe et al., 1990; Pandey et al., 2000; Voleti et al., 2000; Wagstaff et al., 2002; van Doom & Stead, 1997; van Doom, 2001, 2004; van Doom & Woltering, 2005, 2008; Zhou et al., 2005; Eason, 2006; Tripathi & Tuteja, 2007). The present review intends to give an update on the available literature on various strategies of petal senescence and to gain an insight into some important events associated with it.

Flower Senescence

Unlike seeds or fruits, which are single morphological units, flower is a unique organ and is composed of many morphological units such as sepals, petals, androecium, gynoecium, stem and often leaves. These morphologically and physiologically distinct units interact with each other, making the flowers more complex than the other plant organs (Halevy & Mayak, 1979). The process of flower senescence is a correlative one and it occurs at different rates in different parts of a flower, nevertheless these flower components are all connected to each other (van Staden, 1995). Flower senescence is generally rapid and continuous similar to whole plant or leaf senescence (Voleti et al., 2000). An advantage of flower petals, compared to leaves, as a system for studying organ senescence is that the process is irreversible and has tight developmental control. Within a given species it is possible to predict exactly when a bud will open and how rapidly the flower will senesce. In addition, a number of morphological and physiological changes are evident that allow the process to be readily documented. Unlike leaf senescence, flowers have a species specific limited life span which is largely independent of environmental factors, (Rogers, 2006). Life span of the whole flower is regulated for ecological and energetic reasons. The death of individual tissues and cells within the flower is coordinated at many levels to ensure correct timing and is carefully tailored to its ecological requirements. Some floral cells die selectively during organ development, whereas others are retained until the whole organ dies. It is important because the flower can be a substantial sink on the plant's resources, and as such is energetically expensive to maintain beyond its useful life (Ashman & Schoen, 1994).

Strategies of Petal Senescence

Some plants (e.g. Rose, Ranunculus) have distinct sepals and petals in their flower systems while others (Hemerocallis, Nerine, Amaryllis) have undifferentiated sepals or petals called perianth (tepals). In some plants (e.g. Helleborus) petals are absent and the sepals are petaloid which behave as petals (Damboldt & Zimmerman, 1965). Some flower systems (e.g. Consolida, Delphinium) have both sepals and petals but sepals have more ornamental value than petals.

Of all the floral organs, sepals/petals determine the longevity of flowers and sepal/ petal senescence is a distinct factor affecting vase life which is an important determinant of quality of cut flowers. Much attention has therefore been diverted to the physiological, biochemical and genetic processes that occur during petal senescence. Petal senescence is characterized by transient upregulation of numerous genes and down regulation of other genes. Most of the changes in gene expression are related to the remobilization of macromolecules and transport of the mobile compounds out of the petal. Degradation of macromolecules in the senescent cell is mainly due to autophagic processes in the vacuole; protein degradation in mitochondria, nuclei, cytoplasm; fatty acid breakdown in peroxisomes and nucleic acid degradation in nuclei (Bieleski, 1995; Mahagamasekera & David, 2001; Wagstaff et al., 2002; Jones et al., 2005; Narumi et al., 2006; Xu et al., 2006; Chapin & Jones, 2007; Hoeberichts et al., 2007; van Doom & Woltering, 2008; Lerslerwong et al., 2009; Shibuya et al., 2009; Yamada et al., 2009).

The overall pattern of flower or petal senescence varies widely between different genera. Depending on the species, petal senescence is visibly shown by wilting or abscission or even wilting followed by abscission. Wilting is due to turgor loss of petals, whereas withering is a color change and slow dehydration. In species that show wilting of the perianth, an important function of senescence may be to allow remobilization of key metabolites from the senescing organs back into the plant. The metabolites are then directed to the development of other organs such as the developing ovary (Nichols & Ho, 1975; Feller & Keist, 1986; Chapin & Jones, 2007) developing flower buds (Bieleski, 1995) or tuber formation (Fischer et al., 1998). From the available literature, five general patterns of petal senescence can be recognized on the basis how flowers respond to ethylene.

1) Petals exhibiting rapid wilting shortly after the onset of a rise in endogenous ethylene production and treatment with exogenous ethylene dramatically hastens wilting, e.g. carnation and Petunia. If such flowers are treated with inhibitors of ethylene biosynthesis or action, their life is extended substantially (Veen & van de Geijn, 1978; Fujino et al., 1980; Serek et al., 1994).

2) Petals showing slow wilting without any significant rise in ethylene production during the senescence process and that treatment with exogenous ethylene do not have any drammatic effect on flower longevity, e.g. Chrysanthemum, Narcissus, Ranunculus; as such ethylene inhibitors do not increase flower longevity (Nichols, 1966; Stimart et al., 1983; Evans et al., 2002).

3) Petals showing abscission without any visible signs of wilting and abscission is generally stimulated by exogenous ethylene, e.g. Delphinium, Digitalis Purpurea (Shillo et al., 1980; Stead & Moore, 1983). Treatment with ethylene antagonists has been shown to substantially extend the vase life in such type of flowers (Finger et al., 2004).

4) Petals showing abscission which is not stimulated by exogenous ethylene, in that the exogenous ethylene does not induce an autocatalytic production of ethylene and that ethylene antagonists were found to be ineffective in delaying flower abscission e.g. Tulipa, Plectranthus (van Doom, 2001; Ascough et al., 2006).

5) Flowers of some plants such as daffodil exhibit intermediate pattern of senescence (Hunter et al., 2002). Without pollination, their senescence resembles that of ethylene-insensitive flowers, in that there is little ethylene production and only a limited response to inhibitors of ethylene biosynthesis and action. Pollination in such flowers results in an increase in endogenous ethylene production and the application of exogenous ethylene accelerates their senescence.

In flowers of some plant species such as camation, Ranunculus etc. abscission occurs much later than visible symptoms of senescence (Evans et al., 2002) whereas in flowers of plant species such as Tulipa, Alstroemeria and Consolida, abscission occurs almost immediately after the visible signs of senescence (Shillo et al., 1980; van Doom, 2001; Wagstaff et al., 2002). Petals in many species such as Lilium abscise when fully turgid, besides in some species; petals may be more persistent so that cell deterioration and nutrient remobilization occurs while the petals are still part of the flower. In some species as Hemerocallis, the entire flower abscises after the perianth collapses. The difference between the abscission type and the wilting type has been shown to be present at the family level and has been linked to the sensitivity of the flower systems to ethylene (Woltering & van Doom, 1988; van Doom, 2001). The following tables (Table 1 and Table 2) represent the type of senescence and ethylene sensitivity in some selected families of plants as has been recollected on the basis of available literature (Woltering & van Doom, 1988; van Doom & Stead, 1994; van Doom, 2001; Evans et al., 2002; Wagstaff et al., 2002).

Flower senescence in many species is regulated by ethylene and as such a distinction is made, resulting in the recognition of ethylene sensitive and ethylene insensitive flower systems. The difference has been found to correlate with plant families or subfamilies with Orchidaceae, Campanulaceae, Cruciferae, Solanaceae, Scrophulariaceae, Plumbaginaceae, Geraniaceae and Ranunculaceae etc. as 'ethylene sensitive' and Iridaceae, Liliaceae, Amaryllidaceae, Gentianaceae, Euphorbiaceae, Cannaceae etc. as 'ethylene insensitive' families. Except for a few families (Aizoaceae, Campanulaceae, Caryophyllaceae, Solanaceae, Portulacaceae, Lobeliaceae and Malvaceae), most of the flowers that showed initial wilting have been found to be insensitive to exogenous ethylene (Agavaceae, Compositae, Haemodoraceae, Iridaceae, Liliaceae, Umbelliferae, Gentianaceae and Euphorbiaceae) and most of the flowers showing initial abscission have been found to be ethylene sensitive (Acanthaceae, Boraginaceae, Geraniaceae, Gesneriaceae, Labiatae, Ranunculaceae, Rosaceae, Rubiaceae, Scrophulariaceae and Valerianaceae). On the basis of sensitivity to ethylene, plants have been classified into different classes: Class 0 (insensitive to ethylene); Class 1 (up to 33% reduction in vase life on exposure to ethylene); Class 2 (33 to 66% reduction in vase life on exposure to ethylene); Class 3 (66 to 99% reduction in vase life on exposure to ethylene) and Class 4 (immediate drastic effect of ethylene). Ethylene had been found to have little effect on the majority of the wilting types of flowers, however wilting flowers that show high sensitivity to ethylene have been found in 12 of the 42 families investigated.

Ethylene-Sensitive Flower Senescence

Ethylene plays a central role in the senescence of 'ethylene sensitive' flowers, coordinating senescence pathways and regulating floral abscission (Woltering & van Doom, 1988; Trobacher, 2009). A burst of endogenously produced ethylene in such flowers initiates senescence and coordinates the expression of genes required for the process (Woodson et al., 1992; Kende, 1993; Jones et al., 1995; Jones, 2004; Jones et al., 2005; Narumi et al., 2006; Ichimura et al., 2009; Lerslerwong et al., 2009). The pathway of endogenous ethylene production has been shown to be a developmental consequence or induced by pollination (Whitehead & Halevy, 1989; Ketsa & Rugkong, 2000; Wagstaff et al., 2005; Rogers, 2006; Jones, 2008). In flowers of several species such as Petunia, tobacco, carnation and orchids senescence is mediated by the evolution of ethylene following contact between pollen and the stigmatic surface. The exact nature of the primary signal resulting in ethylene evolution has not been established although other PGRs and low molecular weight compounds have been implicated (ONeill, 1997). In carnation, ethylene produced from the pollinated stigma has been shown to be translocated via the style and ovary to the petals where it upregulates ethylene biosynthetic genes and induces the production of ethylene in the petals (Have & Woltering, 1997). The enzymes involved may be transcriptionally regulated by the endogenously produced ethylene leading to a sudden upsurge in autocatalytic ethylene production (Yang & Hoffman, 1984; Woodson & Lawton, 1988; Kende, 1993). It suggests that the promoters of ethylene biosynthetic genes respond to ethylene and contain ethylene responsive elements EREs (Diekman, 1997). The increased ethylene production has been shown to be due to higher amounts of mRNAs for enzymes responsible for ethylene biosynthesis besides; cDNA clones from preclimacteric carnation have been shown to have amino acid sequence with a high homology to ACC synthase (Rottmann et al., 1991; Michael et al., 1993; van Altvorst & Bovy, 1995; Jones & Woosdson, 1999). In carnation autocatalytic rise in ethylene has been found to precede the symptoms of senescence and has been found to be associated with increased transcription of genes encoding enzymes involved in ethylene biosynthesis, such as ACC synthase and ACC oxidase (Park et al., 1992). Genes for enzymes that are also upregulated include a glutathione S-transferase, an S-adenosyl methionine synthase, [beta]-glucosidase, [beta]-galactosidase, cysteine proteases, glutamine synthetase, asparagine synthetase, aspartic proteases, nucleases, monodehydroascorbate reductase and phosphate transporter PhPT1 (Meyer et al., 1991; Raghothama et al., 1991; Woodson et al., 1992; Woodson, 1994; Jones et al., 1995; Panavas et al., 1999; Eason et al., 2000; Wagstaff et al., 2002; Jones et al., 2005; Narumi et al., 2006; Xu et al., 2007; Farage-Barhom et al., 2008; Chapin & Jones, 2009; Tripathi et al., 2009; Yamada et al., 2009). The expression of most of these genes has been found to be controlled by the application of exogenous ethylene supporting the view that their upregulation during senescence is regulated by ethylene. The initiation of autocatalytic ethylene production and the associated increase in gene expression has been suggested to be the result of an increase in the sensitivity of flowers to their continuous low endogenous ethylene levels (Woodson & Lawton, 1988). There is also evidence that petals become more sensitive to ethylene as they age (Lawton et al., 1990). It has been proposed that ethylene may be an effective inducer of senescence only in tissues that have reached a particular developmental stage, besides it has been suggested that the dependence of the ethylene response on the developmental stage of a tissue indicates a mechanism to regulate differential sensitivity to ethylene throughout development (Grbic & Bleecker, 1995; Tiemann et al. 2001). Hunter et al. (2002) also reported that daffodil flowers respond to ethylene only after pollination, before which there is little ethylene production and only a limited response to ethylene, van Doom (2004) however, suggested that it might be due to a decrease in cytokinin levels or to a decrease in soluble carbohydrate levels.

An increase in the production of ethylene has been often found to be a very early post pollination event (Hoekstra & Weges, 1986; Pech et al., 1987; Woltering et al., 1993). During the increase in ethylene production, the styles have been identified as major producers. In orchid Phalaenopsis, the expression of ethylene biosynthetic genes was studied in various flower parts (gynoecium, petals, sepals and labellum) following pollination. ACC synthase and ACC oxidase transcripts were detected in the gynoecium (stigma and ovary) and in the labellum. In the petals and sepals, only ACC oxidase transcripts were detected indicating that ethylene produced by sepals and petals is synthesized from translocated substrate presumably ACC (0Neill et al., 1993). The studies of the expression pattern of ethylene biosynthetic genes in carnation have revealed that the different ACC genes are expressed in a stimulus and organ specific way suggesting that the developing ovary plays a major role in the coordination of the senescence processes that occur in the other flower parts (Woodson et al., 1992; Larsen et al., 1993; Henskens et al., 1994; Woltering et al., 1994). It has been suggested that ethylene presumably acts by binding most probably in a reversible manner to a receptor protein. The ethylene receptor complex then alters the activity of signal transduction reactions, leading to the transcription of specific genes and the synthesis and/or activation of enzymes responsible for physiological effects (Woodson et al., 1992).

The biosynthetic pathway for ethylene has been fully elucidated in higher plants, and plants with mutations that affect the perception or signal transduction of ethylene (Arabidopsis and Lycopersicon) have been used to define the ethylene signalling cascade (ONeill, 1997). Genes that control ethylene production as also ethylene sensitivity and genes that are affected by the presence of ethylene have also been identified in cut flowers (Kosugi et al., 2000; Muller et al., 2002; Shibuya et al., 2002; Verlinden et al., 2002; Shibuya et al., 2004; Lordachescu & Verlinden, 2005). cDNA microarrays have been used to characterize senescence associated gene expression and the results have suggested a master switch during senescence, controlling the coordinated upregulation of numerous ethylene responsive genes of which DC-EIL3 might be a part which gets upregulated during senescence in carnation flowers (Hoeberichts et al., 2007). The expression patterns of ethylene biosynthetic genes have suggested that the regulation of ethylene biosynthesis is controlled by different members of two gene families, ACC oxidase and ACC synthase, both showing tissue specific and developmentally regulated expression (Cornish et al., 1987). The complex regulation mechanisms of ethylene biosynthesis and action have provided with many potential sites where ethylene response can be controlled by chemical treatments or genetic engineering. In rose petals, the expression of ethylene biosynthetic genes (Rh--ASC1-4 and Rh--ACO1) and receptor genes (Rh--ETR 1-5) have indicated that the ethylene biosynthesis in gynoecium is developmentally regulated besides, the response of rose flowers to ethylene occurs initially in gynoecium and that ethylene may regulate flower opening through Rh--ETR3 gene in gynoecium (Xue et al., 2008). Recently an ethylene responsive protease gene RbCP1 has been identified in rose petals that is expressed in response to ethylene (Tripathi et al., 2009). In carnation, ethylene production has been found to be closely correlated with the expression of genes related to ACC synthase CACACC3 and ACC oxidase CARAO1. It was also revealed that ACC synthase gene CARASI though expressed in all flower parts but its activity being either regulated at the transcriptional level or the gene product may require additional factors for activity which presumably may involve ethylene (Have & Woltering, 1997). In Petunia inflata, a cytochrome P450 gene has been recently identified which was found to express at a level 40 times greater in senescing petals than in vegetative tissue. The upregulation has been found to occur in response to compatible pollination, ethylene treatment or jasmonate treatment suggesting its role in the ethylene signalling cascade (Xu et al., 2006). The ethylene signal that initiates senescence in Petunia has been shown to result in the transcriptional activation of the high affinity phosphate transporter PhPT1, which functions in the remobilization of inorganic phosphate during the later stages of senescence (Chapin & Jones, 2009). Phosphate being the most limiting nutrient, this allows the plants to use nucleic acids as phosphorus storage molecules and thereby responding rapidly to senescence signals by remobilizing Pi from unneeded tissues like corollas or older leaves. Evidences so far have supported the involvement of both ethylene dependent and ethylene independent signalling pathways in the Pi responses that lead to increased Pi uptake and reallocation within the plant (Chapin & Jones, 2009).

In species in which ethylene is a major regulator of senescence, ethylene independent signals are also present. Disruption of ethylene signalling or biosynthesis in carnation and Petunia resulted in delayed floral death, but the flowers do eventually die (Michael et al., 1993). It has been suggested that these endogenous signals are active in species where ethylene is not a major regulator. Several transcriptomic studies in Iris and Alstroemeria have revealed the genes or pathways regulating floral disintegration in these species but no clear cut patterns have yet emerged (van Doom et al., 2003; Breeze et al., 2004). It appears that comprehensive studies are needed to understand the response of ethylene biosynthesis and signal transduction.

Involvement of Hormones (Other than Ethylene) in Ethylene-Sensitive Flower Senescence

In ethylene-sensitive flower systems, ethylene undoubtedly plays a major role in promotion of senescence but role of other hormones has also been implicated. Cytokinins have been found to delay floral senescence in carnation, Petunia and roses (Mac Lean & Dedolph, 1962; Mayak & Halevy, 1972; Mayak & Kofranek, 1976; van Staden & Dimalla, 1980; Taverner et al., 1999; Lara et al., 2004). Eisinger (1977)proposed that cytokinins are natural anti-senescence factors and that their declining levels serve as trigger for increased ethylene production. Feeding carnation flowers with 6-methyl purine, an inhibitor of cytokinin oxidase/dehydrogenase, resulted in increased life span of petals suggesting that ethylene promotes inactivation of cytokinins and facilitates the senescence process (Tavemer et al., 2000). Chang et al. (2003) confirmed the role of cytokinins in flower senescence using transgenic approach. The transgenic plants overexpressing IPT gene under the SAG12 promoter was found to exhibit significant delay in flower senescence and corresponding increase in the cytokinin content and less sensitivity to ethylene suggesting that the regulation of flower senescence involves the interactive operation of cytokinins and ethylene. Hoeberichts et al. (2007) have recently reported the increase in mRNA abundance of two genes encoding cytokinin oxidase/dehydrogenase during carnation petal senescence which was found to accelerate cytokinin breakdown and promote corolla senescence.

In ethylene-sensitive flowers such as carnation abscisic acid (ABA) has been found to accelerate flower senescence (Mayak & Dilley, 1976; Ronen & Mayak, 1981). A large increase in ABA levels has been observed in the gynoecium, prior to or concomitant with the ethylene upsurge (Nowak & Veen, 1982; Eze et al., 1986; Onoue et al., 2000). Nowak & Veen (1982) demonstrated that ethylene perception is required for ABA action in carnation as treatment with silver thiosulphate an ethylene antagonist, completely prevented the increase in ABA levels. The removal of gynoecium prevented the induction of ethylene production and early petal wilting by exogenous ABA application, suggesting that the exogenous ABA acts through the induction of ethylene synthesis in the gynoecium (Shibuya et al., 2000; Nukui et al., 2004). Hunter et al. (2004) reported that the premature accumulation of senescence-associated transcripts in the Narcissus tepals is induced by ABA independently of ethylene. The studies implicate the involvement of ABA in both ethylene-sensitive and ethylene-insensitive flower senescence regulating distinct mechanisms which have not been fully elucidated as yet.

The effect of auxins and gibberellins is not well characterized during flower senescence. Auxins have been found to reduce ethylene sensitivity in some tissues while in others they promote senescence by inducing ethylene production. Application of auxins to flowers has been found to stimulate senescence by hastening the rise in ethylene production (Stead, 1992; van Staden, 1995). Jones and Woosdson (1999) reported that 2,4-D a synthetic auxin, induced the expression of ACC synthetase genes in the styles, ovaries and petals. In carnation petals, a transient increase has been observed in the mRNA of an Aux/IAA gene following the application of auxins (Hoeberichts et al., 2007). Gibberellic acid is known to delay senescence in some cut carnation flowers by acting as an antagonist to ethylene (Saks et al., 1992; Saks and & Staden, 1993). In Grevillea, higher levels of gibberellic acid was found to enhance flower abscission rather than senescence (Setyadjit et al., 2006), but the treatment did not enhance the longevity of inflorescences as also the ACC level.

Polyamines (PAs) have been reported as an effective anti-senescence agents and found to retard chlorophyll loss, membrane deterioration and increase in RNase as also protease activities, all of which help to slow the senescence process (Evans & Malmberg, 1989). The major polyamines comprise putrescine, spennidine and spennine, which either occurs naturally or as free bases or bound to phenolics or other low molecular weight compounds or macromolecules (Galston & Kaur-sawhney, 1990). Perez-Amador et al. (1996) reported the accumulation of [N.sup.4]-Hexanoyl spermidine, a polyamine-related compound during the ovary and petal senescence in pea. Exogenous spermidine has been found to transiently delay senescence of Dianthus caryophyllus and Petunia hybrida flowers which has been implicated to be due to the ability of free spermidine to bind to the main intracellular constitutive molecules such as DNA and stabilizing their structures (Lee et al., 1997; Gul et al., 2005; Tassoni et al., 2006).

The role of jasmonates in the senescence of ethylene-sensitive flower systems is not clear as yet. Methyl-jasmonates have been found to accelerate senescence in Petunia hybrida, Dendrobium and Phalaenopsis (Porat et al., 1993, 1995) but in Petunia inflata, only an earlier color change has been reported without any promotion of petal wilting after treatment with methyl-jasmonate (Xu et al., 2006). Genes encoding enzymes of the jasmonate biosynthetic pathway have been shown to be specifically expressed in floral organs (ovaries, petals and sepals) and involved in reproductive processes involving maturation of anthers and release of mature pollen grains (Avanci et al., 2010). The fact that pollination triggers senescence in various flower systems and that jasmonates promote pollen maturation and release, might prove to be a mechanism for role of jasmonates in flower senescence, however more elaborate work is needed to confirm it.

Ethylene-Insensitive Flower Senescence

Ethylene is known to play regulatory role in ethylene sensitive flowers while as in ethylene insensitive flowers abscisic acid (ABA) is thought to be the primary regulator. Exogenous application of ABA to certain flowers has been found to hasten flower senescence (Borochov & Woodson, 1989). ABA is considered to be the primary hormonal regulator of flower senescence in ethylene insensitive day lilies and many of the senescence related changes including ion leakage, changes in lipid peroxidation, protease activity and expression of novel DNases and RNases have been shown to be brought about by ABA (Panavas & Rubinstein, 1998). In Narcissus pseudonarcissus, it has been shown that ABA content increased in tepals of senescent flowers which coincided with the appearance of visible signs of senescence, besides exogenous application of ABA has been found to enhance the premature accumulation of senescence associated transcripts in the tepals indicating that ABA induced the transcripts independent of ethylene (Hunter et al., 2004). It has been reported that PCD in very early stages of tulip petal senescence is triggered by signals other than ethylene, [H.sub.2][O.sub.2] or protease activity and that the intracellular energy depletion is a primary early signal for PCD in tulips (Azad et al., 2008). Some features of apoptosis have been demonstrated in senescence of ethylene insensitive flowers of gladiolus. Using flow cytometry, it has been confirmed that nuclear fragmentation coincided with death in petals after full flower opening (Hoeberichts et al., 2005). Recently PCR-based subtractive hybridization has been successfully used in daffodil and Iris (Hunter et al., 2002; van Doom et al., 2003) to isolate large populations of genes associated with petal senescence. About 54 genes have been isolated from daffodil, including genes encoding a few regulatory proteins and several cysteine and serine proteases (Hunter et al., 2002). Van Doom et al. (2003) have isolated about 51 sequences which include a number of genes with unknown function. The sequences encoding Grap2 and cyclin-D interacting proteins, a MADS-domain transcription factor, a casein kinase and a nucleotide gated ion-channel-interacting protein might be important elements in the regulation of senescence. Regarding the pattern of senescence in ethylene insensitive flowers, the data so far accumulated is scanty and more elaborate work is required to understand the ethylene independent pathway and its execution.

Some Important Events Associated with Petal Senescence

Changes in Membrane Permeability

A consistent feature of senescence is the loss of differential permeability of cell membranes (Thompson, 1988). The permeability and fluidity of biological membranes is modified by variations in the composition and structure of the lipid bilayer (Simon, 1974; Thompson et al., 1998). The physiological consequences of physical and chemical changes in the membrane lipids include modifications in the membrane permeability and loss of membrane bound enzymatic activity (Mazliak, 1981). Biochemical changes involving the membranes include simultaneous decline in all classes of phospholipids and increase in neutral lipids (Paliyath & Droillard, 1992). The changes in the physical properties of the membranes have been suggested to be due to the increased oxidative processes (Shinitzky, 1984; Paulin, 1986).

Deterioration of cellular membranes cause increased membrane permeability, loss of ionic gradients and decreased function of key membrane proteins (e.g. ion pumps). Changes in the properties of membranes such as increase in microviscosity, alterations in saturation/desaturation ratios of fatty acids and peroxidation of lipids, have been known to occur during petal senescence, with a causal link to reactive oxygen species elevated due to stress (Borochov & Woosdson, 1989). Membrane deterioration is commonly associated with progressive decrease in membrane phospholipid content through phospholipase activity. Both lipase and lipoxygenase enzymes have been found to participate in biochemical degradation of lipids and have been linked to the onset of membrane leakiness in various flowers such as carnation and rose (Hong et al., 2000; Fukuchi-Mizutani et al., 2000). It is pertinent to note that loss of membrane function in Alstroemeria has been shown to occur without increased activity of lipoxygenase suggesting that the loss of membrane integrity can be achieved in a number of ways (Leverentz et al., 2000). Paliyath et al. (1987) suggested that combined activities of membrane associated lipoxygenases, phospholipases, phosphatidic acid, diglycerols and free fatty acids may contribute to increasing membrane vesiculation and destabilization. The rapid cessation of overall phospholipid synthesis during Hemerocallis petal senescence has been evidenced (Bieleski & Reid, 1992). During senescence, a massive loss of phospholipids has been observed, concomitant with an increase in the degradation products (Suttle & kende, 1980; Thompson et al., 1998; Hopkins et al., 2007). An increase in gel phase lipid has also been observed in microsomes from carnation petals well ahead of ethylene production and morphological changes (Paliyath & Thompson, 1990). The change from the fluid to gel phase in membranes and a decrease in membrane fluidity has been suggested to be due to enzyme-induced degradation process in the membranes. Freeze-fracture electron microscopy of senescing carnation petals indicated the presence of gel phase lipid in the plasma membrane, endoplasmic reticulum, and tonoplast (Hopkins et al., 2007).

Another senescence-associated event that leads to loss of membrane permeability is the oxidation of existing membrane components. Mayak et al. (1983) observed a reduction in the superoxide dismutase activity during senescence in carnation flowers, with a concomitant increase in free radical levels and in the development of increased lipid peroxidation that paralleled the decrease in membrane fluidity. It has been suggested that the superoxide ([O.sub.2.sup.-]) involved in the conversion of ACC to ethylene is generated by a membrane enzyme and that ethylene production depends on the integrity of the membrane (Mc Rae et al., 1982). In Ipomoea, the loss in membrane integrity has been reported to be due to higher free radical production and consequently a concomitant increase in the viscosity of the cell sap, which corresponded to the mole ratio of free sterol to phospholipid (Beutelmann & Kende, 1977). The effects of free radicals include the induction of lipid peroxidation and fatty acid de-esterification (Kellogy & Fridovich, 1975). According to Mayak et al. (1983), the [O.sub.2.sup.-] anions contribute to phospholipid breakdown and the fatty acids released are then peroxidized and the free radicals produced by peroxidation promotes the burst of ethylene (Paulin et al., 1986).Two cDNA clones from day lily have been sequenced, whose gene products could play a role in oxidizing membrane lipids (Panavas et al., 1999). One clone, detected mainly in petals, has shown the greatest similarity to an in-chain fatty acid hydrolase bound to cytochrome P450. The translated product of this mRNA has been implicated in modifying fatty acids, leading to their degradation (Cabello-Hurtado et al., 1998). The other clone has been found to be similar to an allene synthase, which converts fatty acid hydroperoxides to allene epoxides, and eventually results in molecules that may have signalling capabilities (Song & Brash, 1991).

The proteins too have been shown to cause membrane fluidity during petal senescence. Among the different kinds of proteins, the specific content of thiol groups as well as their total protein content was shown to decrease significantly during carnation petal senescence (Borochov et al., 1982; Borochov & Woodson, 1989). The release of cytochrome C from mitochondria is considered to be a prerequisite for apoptosis (Yang et al., 1997). Following its release the cell dies due to collapse of electron transport, the generation of reactive oxygen species and a reduction in ATP generation (Green, 1998; Yamada et al., 2001). The release of cytochrome C in cytosol has also been reported in zea mays cell suspension following D-mannose treatment (Stein & Hansen, 1999) and in Arabidopsis cell cultures after oxidative stress (Tiwari et al., 2002). It has been reported that the release of cytochrome C in the cytosol and ATP depletion occurs at the early stage of petal senescence and that oxidative stress, ethylene generation and protease activity are evident at the final stages during tulip petal senescence (Azad et al., 2008).

Autophagy

Autophagy during senescence seems to be a main process responsible for cell dismantling and remobilization of macromolecules that can be used in other parts of the plants. It seems to play an essential role in petal senescence. Autophagy may not necessarily be required for cell death. In plants, transport to the vacuole is described by three autophagic pathways of micro- and macro-autophagy (Thompson & Vierstra, 2005; Bassham et al., 2006; van Doom & Woltering, 2005). Microautophagy involves sequestration of the cytoplasm by invagination of tonoplast. Macro-autophagy, by contrast, involves entrapment of proteins of the cytosol by double-membrane vesicles called autophagosomes. The outer membrane of the autophagosomes fuses with the tonoplast to release the internal vesicle as an autophagic body (Thompson & Vierstra, 2005). In cells of senescent Ipomoea petals, an increase in macro-autophagy follows from the presence of numerous vesicles both in the cytoplasm and in the vacuoles (Matile, 1997). The third type of autophagy involves the permeabilization or rupture of the lysosome or tonoplast which appears to be common in plant PCD. It results in the release of vacuolar hydrolases, which can degrade the left-over components of the cell. In petals, the leakage of anthocyanins from vacuoles to apoplast has been suggested to be due to tonoplast and plasma membrane permeabilization (Matile, 2000; van Doom et al., 2003). Van Doom and Woltering (2005) have suggested the name 'Mega-autophagy' to delineate this third type of autophagy.

Although autophagy has been shown to occur during petal senescence (Matile & Winkenbach, 1971; Matile, 1997; Thompson & Vierstra, 2005), the mechanism of autophagy in PCD during petal senescence remains unclear. In the early 1970s, Matile and Winkenbach (1971) suggested that the vacuole acts as an autophage. Invaginations of the tonoplast surround parts of the cytoplasm that are ultimately pinched off, resulting in lysosomal-like compartments within the vacuole. The membrane surrounding these vesicles decay and the cytoplasmic material then appears to be degraded by vacuolar enzymes. Such cytoplasmic degradation has been found to be concomitant with the visible collapse of Ipomoea corolla. Little information is available on the role of autophagy in PCD during petal senescence (Doelling et al., 2002; Hanaoka et al., 2002; Xiong et al., 2005; Bassham et al., 2006; van Doom & Woltering, 2008). Several homologs of yeast (Saccharomyces cerevisiae) autophagy genes, including genes involved in autophagosome formation have been isolated in Arabidopsis thaliana. The expression of genes showing homology to genes involved in animal PCD have also been investigated in Ipomoea (Yamada et al., 2009). In Ipomoea, a putative membrane protein, InPSR26, dominantly expressed in petal limbs has been found to regulate progression of PCD during petal senescence and its transcript level has been shown to increase prior to visible senescence symptoms. Transgenic plants with reduced InPSR26 expression (InPSR26r lines) have showed accelerated petal wilting; with PCD symptoms including cell collapse, ion and anthocyanin leakage, and DNA degradation suggesting that InPSR26 acts to delay the progression of PCD through regulation of autophagic process as transcript levels of autophagy. PCD related genes (InATG4, InATG8, InVPE and InBI-1) were found to be reduced in the petals of transgenic PSR26r plants (Shibuya et al., 2008). The biochemical function of InPSR26 however, remains largely unknown and analysis on the function of this protein may provide new insights on PCD and autophagy in petal senescence. It has been suggested that autophagy is not a cause of PCD but part of the remobilization process as it is essential to the recovery and translocation of nutrients from dying tissue to growing tissues of plants such as developing seeds (Shibuya et al., 2008; Yamada et al., 2009).

Role of Caspases

Caspases are cysteine endoproteases that cleave at aspartate residues. They are important regulators of PCD in animal systems (Cheng et al., 2006; Hail et al., 2006). Plants do not possess true caspases, but do have enzymes with caspases like activity such as vacuolar processing enzymes (VPEs). Although there is limited overall sequence identity between VPEs and caspase-1 but they share several structural properties (Rojo et al., 2003). Four different VPE genes have been isolated and characterized in Arabidopsis (VPE[alpha], VPE[beta], VPE[gamma] and VPE[delta]). VPEgamma] has been found to be localized to vesicles that merge with vacuoles. VPE[beta] and VPE[gamma] have been found to become expressed during leaf senescence, their role in petal PCD is still unknown (Kinoshita et al., 1999; Rojo et al., 2003). VPE[gamma] has been found to be involved in the execution of PCD induced by the bacterium Pseudomonas syringae or the turnip mosaic virus (Rojo et al., 2004). Both VPE[beta] and VPE[gamma] have recently been found to be associated with PCD that is induced by the fungus Botrytis (van Baarlen et al., 2007). VPEs, therefore, seem to be important regulators of developmental and pathogen-induced PCD in plants. VPEs are cysteine proteases that have been found to activate various proteins in the vacuole and are thought to be a key executor of PCD in some type of plant cells (Hatsugai et al., 2006). As VPEs activate several vacuolar proteases, they might be therefore involved in autophagic degradation process and their expression have

been suggested to be regulated in concert without autophagy related genes (Hatsugai et al., 2006).

Degradation of Nucleus and Nucleic Acids

The degradation of nucleic acids (DNA and RNA) has been observed during flower and petal senescence from various plant species such as Pisum sativum, Petunia inflata, Alstroemeria, Gladiolus and Actinidia deliciosa (Orzaez & Granell, 1997a, b; Xu & Hanson, 2000; Wagstaff et al., 2003; Yamada et al., 2003; Coimbra et al., 2004). Some petals have been shown to exhibit DNA degradation rather than classical DNA laddering (Yamada et al., 2006). Using flow cytometry, it has been shown that the number of DNA masses in the petals of Argyranthemum and Petunia markedly increase prior to wilting. However in Antirrhinum, the chromatin fragmented into several spherical clumps and remained inside a large membranous structure (Yamada et al., 2006). Recently Ichimura et al. (2009) reported chromatin condensation and nuclear fragmentation as well as decrease in the DNA content during petal senescence in carnation, regulated by ethylene. Therefore, On the basis of nuclear morphology, PCD could be divided into at least two categories: one involving nuclear fragmentation as in Ipomoea, Petunia and Argyranthemum petals and. the second involving chromatin fragmentation as in snapdragon and carnation petals.

Panavas et al. (1999) cloned a cDNA from daylily petals, with similarity to fungal S1- and P-type endonuclease that degrades both single-stranded DNA and RNA. The transcript level of this putative nuclease was found to increase at flower opening and continued to increase during senescence. Five DNases with specific activity against ssDNA have been identified from petals of Petunia and all of them have been shown to increase during the senescence of pollinated flowers but so far a single cobalt-dependent senescence-specific nuclease, PhNUC1 has been characterized (Langston et al., 2005). Activity of PhNUC1 has been found to be induced in non-senescing corollas by treatment with ethylene and was found to delay in ethylene-insensitive mutants (35S: etrl-1) suggesting that regulation of DNA fragmentation and nuclease activity through PhNUC1 is ethylene-dependent. Recently a cDNA fragment, encoding a putative nuclease (DcNUC1) has been isolated from the petals of senescing carnation flowers whose transcripts were also found to be upregulated corresponding to the increase of ethylene production (Narumi et al., 2006).

Almost forty years before Winkenbach had reported a decline in RNA levels by the time of onset of Ipomoea flower opening. The levels of RNA were found to decrease further as the flower opened and were found to be accompanied by a dramatic upsurge of RNase activity (Winkenbach, 1970a, b). Treatment of Ipomoea flowers with ethylene resulted in earlier inward rolling of the corolla and an earlier increase in RNase activity (Kende & Baumgartner, 1974) suggesting that regulation of RNA fragmentation is ethylene- dependent. RNase activity has also been found to increase during petal senescence in such flowers as Hemerocallis (Panavas et al., 2000).

Protein Synthesis and Degradation

Protein synthesis and degradation are the events of central importance during petal senescence. Treatment of flowers with compounds that inhibit protein synthesis, have been found to delay the visible symptoms of petal senescence, revealing that active protein synthesis is required for the execution of cell death in petals (Lay-yee et al., 1992; Celikel & van Doom, 1995; Sultan & Farooq, 1997; Wagstaff et al., 2002; Xu et al., 2007; Shahri & Tahir 2010). The ultrastructural data indicates that floral abscission too requires high protein synthesis and secretory activity of material towards cell walls of the abscission zone cells (van Doom & Stead, 1997). van Doom et al. (2004) has reported that an active alkaloid 'Narciclasine' from Narcissus (daffodil) delayed the tepal senescence of cut iris flowers by inhibiting protein synthesis, thereby leading to the same conclusion. Several genes related to protein synthesis have been found to be differentially expressed during petal senescence (van Doom & Woltering, 2008). The degradation of proteins and the remobilization of amino-acids to developing tissues is a prominent process during senescence (Bieleski, 1995; Solomon et al., 1999). Protein breakdown occurs in proteasomes, vacuoles, mitochondria, nucleus and plastids but bulk degradation mainly occurs in vacuoles (van Doom & Woltering, 2008). A continual turnover of proteins removes functionally impaired proteins (due to biosynthetic errors, improper folding, thermal denaturation and oxidative damage), which if left unchecked may restrict metabolic activities. Proteolysis also recycles essential amino acids and is important for the recovery of essential nutrients (Clarke, 2005). Proteolysis is thought to play a significant role in the senescence of flowers because expression of protease genes is one of the earliest senescence-related gene changes to be identified (Eason et al., 2002). Upregulated expression of protease genes, raised enzymatic activity and a decline in soluble protein levels have been found to occur consistently during senescence, both in ethylene sensitive and ethylene-insensitive flowers (Panavas et al., 1999; Eason et al., 2002; Wagstaff et al., 2002; Jones et al., 2005). Large losses in the protein levels during senescence have been reported prior to wilting in such flowers as Ipomoea, Hemerocallis and Petunia (Matile & Winkenbach, 1971; Lay-yee et al., 1992; Sultan & Farooq, 1996; Gulzar, 2003). A slight reduction in total protein content of petal tissues has been observed during senescence in flowers such as Consolida, Digitalis and potted Chrysanthemum prior to abscission suggesting that the extent of protein loss is least in species showing petal abscission rather than wilting (Stead & Moore, 1983; Williams et al., 1995; Shahri & Tahir, 2010). The decrease in protein levels has been suggested to be due to decreased synthesis and/or increased degradation (Celikel & van Doom, 1995). The net protein degradation has been found to occur early in Iris tepals during the senescence process (Celikel & van Doom, 1995) whereas in Hemerocallis, a sharp decrease in protein levels has been shown to precede the visible symptoms of senescence (Lay-yee et al., 1992). Cycloheximide has been shown to delay the decrease in protein levels and inturn increase the time to visible senescence suggesting that protein degradation may lead to senescence symptoms (Courtney et al., 1994).

Protein turnover is mediated through proteasomes and various classes of proteasome-independent proteases whose transcripts have been found to accumulate in senescing floral tissues (Cervantes et al., 1994; Jones, 2004; Jones et al., 2005). Proteasomes have been found to be involved in degradation of specific proteins particularly misfolded proteins (reviewed in van Doom & Woltering, 2008). The level of other important transcriptional regulators such as those involved in auxin and gibberelin responses are also determined by proteasomal action (Bisshopp et al., 2006). The degradation of proteins via proteasome pathway is mediated by the ubiquitination of proteins prior to degradation and subsequent cleavage by specific protease enzymes (Courtney et al., 1993). The proteasome mediated protein degradation has been found to be upregulated during petal senescence in daylily (Courtney et al., 1994), daffodil (Hunter et al., 2002), and carnation (Hoeberichts et al., 2007). However in Alstroemeria, very little change in the expression of putative ubiquitin cDNA, ALSUQ1, has been observed during flower development and senescence suggesting the existence of alternative pathway for proteolysis (Wagstaff et al., 2002). The delay of visible senescence symptoms after chemical inhibition of proteasomes in Iris and after-silencing a RING domain E3 protein in Petunia indicates that proteasome action is required for proteolysis in these flower systems (reviewed in van Doom & Woltering, 2008).

Proteasome independent protease activity has been found to increase prior to visible senescence (Stephenson & Rubinstein, 1998; Pak & van Doom, 2005). Non-proteasome proteases have been divided into exopeptidases and endopeptidases depending on the cleavage position of target proteins. Using class-specific protease inhibitors and gelatin polyacrylamide gel electrophoresis, different classes of senescence-associated endopeptidases have been partially characterized in broccoli florets (Wang et al., 2004). The proteases were separated into seven endoprotease (EP) groups and classified into metalloproteases (EP1), metallo- and cysteine proteases (EP2), serine- and aspartic proteases (EP3), cysteine proteases (EP4, EP5 and EP7) and serine proteases (EP6) based on the sensitivity to class-specific protease inhibitors. Reports have confirmed that serine protease activity contributes to early stages and later stages of flower development and that cysteine and aspartic protease activities participate throughout flower senescence in broccoli (Wang et al., 2004). Among all the proteases, cysteine proteases are the most frequent and well characterized (Stephenson & Rubinstein, 1998). Several cysteine proteases have been shown to be upregulated and characterized from petals of carnation, Hemerocallis, Alstroemeria, Narcissus, Sandersonia, Gladiolus and Petunia (Jones et al., 1995; Valpuesta et al., 1995; Guerrero et al., 1998; Eason et al., 2002; Hunter et al., 2002; Wagstaff et al., 2002; Arora & Singh, 2004; Jones et al., 2005).

Cysteine proteases are comprised of a number of different classes, but the majority of senescence-associated cysteine proteases behave as typical Papain family members (Granell et al., 1998). Several senescence-associated cysteine protease genes have been reported to increase in abundance following ethylene treatment (Cervantes et al., 1994; Alonso & Granell, 1995; Jones et al., 1995; Weaver et al., 1998; Cercos et al., 1999; Jones et al., 2005; Tripathi et al., 2009). In Petunia, nine different cysteine protease genes have been identified that were found to express in corollas. Three of the nine cysteine protease genes (PhCP4, PhCP6 and PhCP7 were found to be down-regulated whereas six other protease genes (PhCP2, PhCP3, PhCP5, PhCP8, PhCP9 and PhCP10) were upregulated during the natural senescence of corollas. The pattern of decreasing mRNA abundance in PhCP4, PhCP6 and PhCP7 during flower ageing suggests that the group of proteins is most likely to be involved in the regulation of general protein turnover and cellular maintenance during the growth and development of the petals. PhCP6 was found to show high homology to cysteine protease from castor bean and other KDEL-containing proteases. It has been suggested that cys EP-like proteases in Petunia corollas are not likely to be involved in the large scale proteolysis that accompanies the latter stages of petal senescence, but may be involved in processes early in flower development that involve PCD (Jones et al., 2005). The majority of the cysteine protease genes from Petunia have been found to exhibit senescence-associated increases in transcript abundance suggesting their major role during senescence in catalyzing the large scale degradation of proteins that accompanies petal wilting. PhCP10 has been found to be the only senescence-associated protease that had a senescence-specific expression whose transcripts were detected only in senescing petals, styles and leaves and was found to have high homology to SAG12 from Arabidopsis and SAG12 homologues from tobacco and Brassica napus (Jones et al., 2005). It is concluded that cysteine protease gene expression in Petunia is developmentally regulated and that PhCP10 can be used as an excellent molecular marker for petal senescence. Partial cDNAs of ubiquitin (ALSUQ1) and a putative cysteine protease (ALSCYP1) have been cloned from Alstroemeria. A dramatic increase in the expression of ALSCYP1 has been observed during senescence indicating that the gene encodes an important enzyme for proteolytic process. In addition, three papain class cysteine protease enzymes showing different patterns of activity during flower development have been identified on zymograms, one of which has been found to show a similar expression pattern to cysteine protease cDNA (Wagstaff et al., 2002). Recently, a cysteine protease gene, RbCP1, has been identified that was found to encode a putative protein of 357 amino-acids and was found to express in the abscission zone (AZ) of rose petals. The gene has been found to be responsive to ethylene and its transcript accumulation was found to be accompanied by the appearance of a 37 KDa cysteine protease, a concomitant increase in protease activity and a substantial increase decrease in total protein content in the abscission zone of rose petals (Tripathi et al., 2009).

In certain cut flowers (Sandersonia and Iris), chemical inhibition of protease action has been found to delay the onset of senescence (Eason et al., 2002; Pak & van Doom, 2005). Sugawara et al. (2002) have cloned a gene from carnation flower for the cysteine protease inhibitor that was found to express abundantly in the petals at the full opening stage of the flower and its expression was found to decline temporarily during senescence suggesting that it plays an important role in the regulation of petal senescence by fine tuning the expression of different cysteine proteases. PCD promoting signals have been suggested to induce inactive zymogens to active proteases, and trigger irreversible proteolysis cascade leading to cell death (Stephenson & Rubinstein, 1998).

In addition to cysteine proteases, other types of endopeptidases have been suggested to be involved in flower senescence. Guerrero et al. (1998) reported a cDNA clone encoding a daylily thiol protease (SEN11) whose expression was strongly found to upregulated in flower tepal senescence. The elevated expression of a thiol protease TPE4A has also been reported during senescence of unpollinated pea ovaries (Cercos et al., 1999). Azeez et al. (2007) reported the expression of specific serine proteases during senescence-associated proteolysis in Gladiolus flowers. It was found that the activity of some serine proteases increase up to 2/3 of total protease activity during senescence. Chloroplasts, non-chloroplast plastids and mitochondria have been found to contain several families of ATP-dependent proteases (called Clp, Lon and FtsH) and one family of ATP-independent proteases (called DegP). The Clp, Lon and DegP families have been found to belong to serine proteases and the FtsH family to metallo-proteases (Sinvany-villallobo et al., 2004). The transcript abundance of Clp proteases have been increases prior to visible senescence. Dominguez & Cejudo (2006) reported the transcript abundance of non-proteasomal serine proteases from plant nuclei which have been suggested to be involved in the degradation of nuclear proteins during senescence.

Exopeptidases have also been shown to play an important role in petal senescence and the levels of exopeptidase and endopeptidase activities have been found to be developmentally regulated (Mahagamasekera & David, 2001). The exopeptidase (leucine aminopeptidase) activity was found to increase several hours earlier than the endopeptidases suggesting that exopeptidases may play a role in protein turnover during flower opening and in the initiation of protein hydrolysis associated with petal senescence while the endopeptidases could be responsible for the breakdown of the bulk of proteins at the later stages (Mahagamasekera & David, 2001).

Remobilization of Essential Nutrients

During petal senescence, the programmed degradation of macromolecules and remobilization of essential nutrients have been observed that allows the plant to remobilize nutrients from dying or senescing tissues to developing tissues (Hew et al., 1989; Jones, 2004; Stead et al., 2006). Hew et al. (1989) reported the movement of phosphorus and soluble amino nitrogen out of the petals of Arachnis orchids via phloem. Changes in the mineral nutrient content of Petunia corollas have indicated that nitrogen, phosphorus and potassium are remobilized during the natural senescence of unpollinated flowers. Corolla phosphorus levels have been found to decline by 75% while as nitrogen and potassium content declined by only 50% and 40% respectively (Matile & Winkenbach, 1971; Verlinden, 2003). Inorganic phosphate seems to be mainly derived from degradation of proteins, phospholipids, and nucleic acids. In the vacuole phosphates have been shown to be remobilized by enzymes such as phosphatase and phosphodiesterase (Matile, 1997). Recently a high-affinity phosphate transporter, PhPT1 has been cloned from senescing petunia corollas and its expression was found to be upregulated during corolla senescence in response to ethylene (Chapin & Jones, 2009). It functions in the remobilization of inorganic phosphate ([P.sub.i]) during the later stages of senescence (Chapin & Jones, 2009). Since phoshorus can be the most growth limiting nutrient, this allows the plant to use nucleic acids as phosphorus storage molecules and to respond rapidly to senescence signals by remobilizing [P.sub.i] from unneeded tissues like corollas or older leaves. It has been postulated that the signaling pathways that function during [P.sub.i] starvation in the shoot and root are distinct from those that function in [P.sub.i] remobilization during natural senescence of leaves and petals (Chapin & Jones, 2009). Nitrogen is exported from the senescing tissues via phloem in the form of amino-acids glutamine and asparagine (Kamachi et al., 1992). Both glutamine synthetase and asparagines synthetase genes whose protein products catalyze the conversion of ammonium to glutamine and asparagine respectively have been identified in senescing leaves and petals, supporting their role in nitrogen remobilization (Buchanan-wollaston & Ainsworth, 1997; Eason et al., 2000). Carbon levels have been found to decrease during leaf and petal senescence (Himelblau & Amasino, 2001; Verlinden, 2003) but it remains unclear whether this is the result of carbon recycling or increased tissue respiration.

Additional nutrients, including chromium, copper, iron, zinc, molybdenum and sulphur have also been found to be remobilized during the senescence of Arabidopsis leaves (Himelblau & Amasino, 2001). Many enzymes contain metals like copper and zinc, which are released during protein degradation. Metallothioneins are known to bind copper and zinc ions (Hall, 2002). The increase in the expression of genes encoding metallothioneins during petal senescence have been related to metal transport besides other alternative roles including detoxification of reactive oxygen species (ROS) and prevention from accumulation of toxic levels of ionic copper in living tissues (Kiningham & Kasarskis, 1998; Hunter et al., 2002; Breeze et al., 2004; Balamurugan & Schaffner, 2006).

The nutrient changes during pollination induced corolla senescence have been investigated in Petunia corollas (Chapin & Jones, 2007). Plant macro and micronutrients as also other additional elements have been measured from non-senescing corollas and compared to levels in corollas at the advanced stages of senescence. Elements like carbon, nitrogen, phosphorus, potassium, sulphur, iron, molybdenum and zinc have been found to be reduced in corollas during pollination-induced senescence while carbon, nitrogen, phosphorus and copper were found to be reduced in corollas during the senescence of unpollinated flowers, suggesting that a different nutrient remobilization programme operates during pollination-induced senescence. This has been suggested to be due to the different sink tissues as the nutrients in pollinated flowers are likely to be remobilized to the developing ovary while in unpollinated flowers nutrients are being transported to sink tissues outside of the flower (Chapin & Jones, 2007). Carbohydrates have been shown to be mainly transported in the phloem during petal senescence (van Doom & Woltering, 2008). sucrose is suggested to be the principal sugar in the phloem exudates in daylily (Bieleski 1995) but hexoses have also been found to be translocated during petal senescence (van Doom & Woltering, 2008).

Many genes putatively involved in macromolecule and organelle degradation has been identified in screens (Buchanan-wollaston et al., 2003; Jones, 2004; Stead et al., 2006) but comparatively little is known about the genes whose products facilitate nutrient remobilization from senescing tissues. In Alstroemeria, syntaxin gene has been found to be upregulated which showed a high homology with Arabidopsis SYP81 (Uemera et al., 2004). Large scale profiling in Arabidopsis has identified a number of transport proteins including phosphate transporters, which were found to be upregulated during natural leaf senescence (van der Graaff et al., 2006). By contrast, only one putative phosphate transporter, PhPT1 recently cloned from Petunia corollas has been found to be upregulated during petal senescence (Chapin & Jones, 2009).

There is significant evidence that the nutrient remobilization is the central role of senescence, as many senescence-enhanced genes in both leaves and petals encode for catabolic enzymes involved in the breakdown of macromolecules and cell organelles (Jones, 2004; van Doom & Woltering, 2008).

A schematic model representing some important events associated with petal senescence (Recollected from the available literature discussed in the review article).

[ILLUSTRATION OMITTED]

Summary

1. Five different classes of petal senescence have been recognized on the basis of sensitivity of flowers to ethylene and their symptoms of senescence i.e. wilting or abscission.

2. A large number of plant families have been found to consist of both ethylene-sensitive and ethylene-insensitive flower systems, thereby suggesting that ethylene sensitivity should not be assigned at the individual level rather than at the family level.

3. Although Ethylene is known to play a major a role in the senescence of ethylene-sensitive flowers but the exact nature of the primary signal resulting in ethylene production is still not clear. Ethylene found to be developmentally regulated exercises its effect by regulating the transcription of a large number of genes. Although the biosynthetic pathway of ethylene has been fully elucidated in higher plants, comprehensive studies are required to understand its response and signal transduction as other hormones might be acting synergistically or antagonistically to bring out the response.

4. In ethylene-insensitive flower systems, ABA is thought to be an important regulator of petal senescence. The data so far accumulated is scanty and needs more elaborate studies to understand the execution of ethylene-independent pathways in both ethylene-sensitive and ethylene-insensitive flower systems.

5. Autophagy plays an important role in petal senescence as it has been implicated in cell dismantling and remobilization of essential nutrients from senescing petals/sepals to developing floral parts. Three different autophagic pathways have been described in plants. VPEs seem to be important regulators of developmental and pathogen-induced PCD in plants and their expression has been found to be regulated in concert without autophagy related genes suggesting that cellular autophagy can be achieved in a number of ways.

6. Petal senescence is accompanied with the degradation of nucleic acids as well as nucleus. The literature so far accumulated is however scanty to provide a detailed information on the temporal regulation and its signalling cascade, although vacuolar rupture is one of the factors suggested to be involved.

7. Protein turnover (de novo synthesis and degradation assumes the central importance during petal senescence as decline in soluble protein levels has been found to occur consistently in both ethylene-sensitive and ethylene-insensitive flower systems. Protein degradation is mediated through proteasomes or through different classes of proteasome-independent proteases. Among the proteases, cysteine proteases have been well characterized and characterized into a number of classes. Several genes related to protein synthesis and degradation has been found to be differentially expressed during petal senescence.

8. Many genes putatively involved in macromolecule and organelle degradation has been identified in screens but comparatively little is known about the genes whose product facilitate nutrient remobilization. Recently a phosphate transporter gene PhPT1 has been cloned which was found to be upregulated during petal senescence.

9. Although some important events associated with petal senescence has been represented diagrammatically interacting in a number of ways to bring out the cell death, there are a number of missing links which needs to be addressed and incorporated appropriately so as to make it a representative model of petal senescence.

Acknowledgements The authors thank Prof. G. H. Dar, Head Department of Botany, for his cordial support. Waseem Shahri thanks University Grants Commission, India for providing Junior Research Fellowship.

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DOI 10.1007/s12229-011-9063-2

Waseem Shahri (1,2) * Inayatullah Tahir (1)

(1) Department of Botany, University of Kashmir, Srinagar, India 190006

(2) Author for Correspondence; e-mail: waseem.bot@gmail.com

Published online: 4 May 2011

[c] The New York Botanical Garden 2011
Table 1 Senescence symptoms and ethylene sensitivity of some monocot
families

Monocot families   Senescence symptoms   Sensitivity to ethylene

Agavaceae          W                     0
Alismataceae       W                     4
Amaryllidaceae     W/WA                  0-3
Cannaceae          W                     0
Commelinaceae      W                     3-4
Haemodoraceae      W                     0
Iridaceae          W/A                   0-4
Liliaceae          W/A                   0-3
Orchidaceae        W                     3-4

Table 2 Senescence symptoms and ethylene sensitivity of some dicot
families

Dicot families      Senescence symptoms   Sensitivity to ethylene

Acanthaceae         A                     4
Aizoaceae           W                     3-4
Boraginaceae        A                     4
Campanulaceae       W                     2-4
Caprifoliaceae      A/W                   0-4
Caryophyllaceae     W                     4
Compositae          W                     0-1
Convolvulaceae      W                     4
Crassulaceae        W                     0-2
Cruciferae          A/W                   2-4
Dipsaceae           W/WA                  2-3
Ericaceae           W/A                   0-4
Euphorbiaceae       W                     I
Fumariaceae         WA                    2
Gentianaceae        W                     0
Geraniaceae         A                     4
Gesneriaceae        A                     4
Labiatae            A                     4
Lobeliaceae         W                     2-3
Malvaceae           W                     4
Oleaceae            A                     4
Papavaraceae        A                     4
Plumbaginaceae      W                     3-4
Primulaceae         A/W/WA                2-4
Portulacaceae       W                     3-4
Ranunculaceae       A/WA                  0-4
Rosaceae            A                     3-4
Rubiaceae           A                     3-4
Saxifragaceae       A/W/WA                0-4
Scrophulariaceae    A                     3-4
Solanaceae          WA/W                  3-4
Umbelliferae        W                     0
Valerianaceae       A                     3-4

A Abscission, W Wilting, WA Wilting followed by abscission
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Date:Jun 1, 2011
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