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The Role of Growth Regulators in Senescence
C H A P T E R
6 The Role of Growth Regulators in Senescence Imran Haider Shamsi⁎, Tichaona Sagonda⁎, Xin Zhang†, Gerald Zvobgo⁎, Heren Issaka Joan⁎ ⁎
Department of Agronomy, Institute of Crop Science, Zhejiang University, Hangzhou, People’s Republic of China †School of Marxism, Zhejiang University, Hangzhou, People’s Republic of China
1 INTRODUCTION The final stage of leaf development, termed senescence, includes programmed cell death (PCD). The timing and occurrence of senescence in plant species and genotypes are influenced by a number of factors. Because developmental senescence is initiated regardless of the normal growth of the plant, it is possible that the process is genetically programmed. Thus, the process of senescence can be described further as genetically programmed cell death (PCD) that is extensively controlled by multiple layers of regulation, including translational and posttranslational regulation (Gan and Amasino, 1997). Senescence occurs in specific organs or in the organism as a whole, with grains like rice and wheat exhibiting its effects during their harvest periods, in contrast, the leaves of deciduous trees change from green to yellow in autumn, an indication of organ-specific senescence (Yoshida, 2003). Leaf senescence is required for plant survival because as old leaves degrade, their products are translocated to young leaves, which will serve as nutrients (Himelblau and Amasino, 2001). Due to the complexity and orderliness of events in senescence, it is clear that the process is not controlled by a single factor, but rather by several factors, including low nitrogen (Islam et al., 2017), high sugar content (Masclaux et al., 2011), cold stress, salinity stress, and plant growth regulators (PGRs).
Senescence Signalling and Control in Plants https://doi.org/10.1016/B978-0-12-813187-9.00006-8
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2 PLANT GROWTH REGULATORS The term PGR has been widely used to describe any substance that can be used to regulate the growth of a whole plant or a specific part of a plant, regardless of the source of production. However, a clear distinction needs to be made between plant hormones and exogenously produced PGRs. Plant hormones are naturally produced signal molecules that operate under minute concentrations, while PGRs are synthetic chemicals used to alter the growth of plants. The most common naturally produced hormones include abscisic acid (ABA), jasmonic acid (JA), salicylic acid (SA), cytokinins (CKs), auxin, gibberellic acid (GA), and ethylene. PGRs act as natural plant hormones, with their biological activity similar to or exceeding that of the equivalent endogenous hormones. Apart from natural plant hormones, other natural growth substances exist, such as brassinosteroids (BRs), oligosaccharides, systenins, polyamines, phosphoinositosides, and SA, all of which are responsible for altering the growth of plants via a number of mechanisms. Natural growth substances, along with PGRs, may alter the synthesis, destruction, activation, and sensitivity to the equivalent natural plant hormones or other types. Thus, in this chapter, we will use the term PGR to refer to any chemical that stimulates or inhibits plant growth, regardless of its site of production. Due to the complexity of the regulation process, PGRs function by themselves or in combination with other classes of PGRs, whether simultaneously or sequentially. In addition to inducing senescence, PGRs alter the formation of flowers and leaves and initiate fruit ripening. The function and interaction of PGRs with various transcriptional factors and their cross-talk among each other stand out, principally due to their roles in plant senescence. Thus, it is imperative to outline the importance of and the regulatory mechanism of PGRs in senescence.
3 PGRS IN SENESCENCE The role of senescence is to facilitate the remobilization of nutrients from moribund parts to actively growing parts. PGRs utilize both environmental and developmental cues to enable senescence to acclimatize the plant to a wide range of environmental conditions so as to extract the maximum amount of nutrients from the moribund tissues. Because of their varying structures, PGRs play a number of possible roles in plant senescence, with some such as ABA, JA, and SA inducing senescence, while CK, auxin, and GA elucidate a contrasting response. Over the past decade, in-depth studies have been done on the functions of PGRs in regulating senescence, including auxin, ethylene (Wu et al., 2017), JA (He et al., 2002), ABA (Song et al., 2016), and SA. In addition, various studies have outlined the cross-talk among various PGRs (Kim et al., 2011; Hu et al., 2017) while regulating plant senescence, and all of the findings agree on the functions of PGRs in senescence. PGRs regulate senescence in multiple ways, with some not directly involved in the regulation of senescence, but rather working antagonistically with other PGRs (Jibran et al., 2013), while others regulate the progression rather than the onset of senescence. In addition, some defense-related PGRs, like SA, JA, and ethylene, tend to accumulate more in the final stages of leaf senescence due to their role in protecting plants from biotic stress because older leaves are more prone to the vagaries of biotic stress.
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The underlying question would be about how PGRs modulate senescence. PGRs are very important in plant development and adaptation to stress, and thus they are crucial in senescence because senescence is a developmentally regulated process modulated by stress (Jibran et al., 2013). PGRs influence leaf senescence in all the plant development stages—that is, by affecting leaf developmental stages, influencing environmental signals, and regulating the speed of senescence once the leaf has initiated the process (Jibran et al., 2013). They are responsible for signal regulation of stress-related genes, senescence-associated genes (SAGs), and transcription factors that are essential for plant survival and growth. The WRKY family of transcription factors stands out as an important group of substances that PGRs regulate in senescence. The PGRs regulate the WRKY in a series of events that has been proposed by Besseau et al. (2012), including the expression of negative regulators before leaf senescence, and then they simultaneously induce positive and negative regulators at the beginning of senescence following positive regulation during the senescence. Studies in knockout mutant and overexpressing lines have shown inhibition or enhanced cell death in natural environments upon the exogenous application of PGRs. Furthermore, under stressful conditions, exogenous application of other PGRs has been shown to reduce a plant’s tolerance to abiotic stress (Shi et al., 2012), while other PGRs like SA increase this tolerance (Canakci and Dursum, 2012). PGRs function in acclimatization to various abiotic stresses by regulating the sensitivity and responsiveness of tissues. It is also noteworthy that the process of senescence is induced at a certain developmental stage, and thus the effects of some of the PGRs also depend on leaf maturity, with the supply in mature leaves inducing the onset of senescence, while the same does not occur in young leaves (Jing et al., 2002). Taken together, one can postulate that PGRs like auxins and BRs are modulators of plant development, while JA, SA, and BA respond to stress and other environmental signals. Thus it is clear that the role of each PGR needs to be elucidated to understand its precise role in senescence. Therefore, this chapter will give an outline of the regulation of senescence, focusing on the commonly known PGRs, their functions, current findings, and their crosstalk with each other. Although many studies have focused on individual PGRs, it is important to note that PGRs communicate with each other in regulating senescence, with some working to antagonistic effect and others cooperating with each other. Due to overlapping of PGRs in their mode of action, the regulation of senescence by PGRs is a complex mechanism that needs deeper understanding.
3.1 Jasmonic Acid and Senescence Jasmonates are derived from beta-linolenic acid, and they regulate various plant growth and development stages, such as fertility, anthocyanin production, root growth, seed germination, senescence, and plant defense mechanisms against biotic and abiotic stress (Kim et al., 2015; Jibran et al., 2013). JA was first reported as a hormone when methyl jasmonate (MeJA) was shown to induce senescence in wormwood and detached oat (Avena sativa) leaves (Kim et al., 2015; Gan, 2010; He et al., 2002). The biosynthesis of JA is catalyzed by several enzymes, such as allene oxide synthases (AOSs), allene oxide cyclases (AOCs), 12-oxo-phytodienoic acid (OPDA) reductases (OPRs), and acyl-CoA oxidases (ACXs) (Fang et al., 2016). JA carboxy methyl transferases (JMTs) and jasmonoyl isoleucine conjugate synthases (JARs) are included in the generation
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of bioactive forms, MeJA, and jasmonate-isoleucine (JA-Ile; Fang et al., 2016). Two main pathways exist for JA biosynthesis, with one localized in the chloroplast and the other localized in the cytoplasm; and both have alpha-linolenic acid as the first compound in the JA biosynthetic pathway. Evidence of the pathway localized in the cytoplasm is provided by a functional study involving overexpression of a cytosolic AOS in tobacco (Nicotiana tabacum) (He et al., 2002). Recent studies in Arabidopsis show that JA is involved in leaf senescence, and this is demonstrated by mutation studies of the JA synthesis and receptor genes, as well as studies measuring plant responses to JA and its many derivatives. For example, temporal shifts in the start of natural and dark-induced senescence have been observed in Arabidopsis plants, with mutations that result in reduced JA levels and make the mutants insensitive to JA (Kim et al., 2015). Early onset of senescence in attached and detached leaves also has been observed in wild-type Arabidopsis treated with exogenous JA at 30 μM, but the same treatment fails to induce senescence in JA-insensitive mutants. This seems to indicate that the JA-signaling pathway is required in order for JA to promote leaf senescence (Gan, 2010). JA biosynthesis genes have been reported to be differentially expressed during leaf senescence, with JA concentrations four times higher in senescing leaves than in nonsenescing leaves (Gan, 2010; Kim et al., 2015; Criado et al., 2007). A number of studies have concluded that synthesis of JA during leaf senescence could be a secondary by-product from the breakdown of macromolecules and membranes in the process of senescence (Kim et al., 2015). However, contradicting results have been reported regarding the role of JA in dark-induced senescence from studies looking at a range of mutants in JA biosynthesis and signaling (Jibran et al., 2013). Delayed dark-induced leaf senescence has been shown in JA-signaling-impaired mutants (such as coil-2) and reduced jasmonate content mutants via silencing of the beta- oxidation gene 3-Ketoacyl-CoA Thiolase-2 (KAT2). However, delayed dark-induced senescence is not observed in other mutants, such as AOS and oxophytodienoic acid reductase (OPR3; Jibran et al., 2013).
3.2 Ethylene and Senescence Ethylene is an important phytohormone that affects a number of plant development processes, including fruit ripening, cell division, abiotic and biotic stress response, cell elongation, and senescence. For example, mutant plants, in which ethylene signaling is overexpressed, show higher survival rates under salt stress when compared to wild-type plants (Jibran et al., 2013). Also, overexpression of the ethylene-inducible transcription factor AtEBP in tobacco stops cell death caused by exposure to hydrogen peroxide (H2O2), and heat (Jibran et al., 2013). Ethylene production is also increased in response to water stress, mechanical wounding, and biotic stresses (Pandey et al., 2000). Ethylene is synthesized from methionine via a pathway involving the conversion of S-adenosylmethionine (SAM) to a cyclic amino acid, 1-amino cyclo propane-1-carboxylic acid (ACC) catalyzed by ACC synthase, with the intermediate being converted to ethylene by oxidation of ACC oxidase (Pandey et al., 2000). The senescence-promoting properties of ethylene were first observed in leaves and stems exogenously treated with ethylene (Ferrante and Francini, 2006). These experiments showed that ethylene treatment induced typical leaf senescence symptoms, including chlorophyll,
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protein, and macromolecule degradation, as well as an increase in catabolic enzymatic activity (Gan, 2010). However, leaf maturity determines the extent to which ethylene can speed up the senescence of leaves. Ethylene in mature leaves leads to an early start of senescence, while it does not do so in young leaves (Jibran et al., 2013). The regulatory mechanism of ethylene during senescence was unknown until recent studies in Arabidopsis shed much needed light (Kim et al., 2015). Delayed senescence was observed in the leaves of an ethylene- insensitive mutant of Arabidopsis (Etr1). The etr1-1 mutation inhibits the receptor from binding ethylene, making the mutants insensitive to ethylene (Gan, 2010). This experiment lends support to the promoter role of ethylene in senescence. In addition, certain Arabidopsis mutant lines with ethylene signaling-defective genes (ein2), which renders the mutants insensitive to ethylene, showed delayed senescence (Buchanan-wollaston et al., 2003; Gan, 2010). Other transcriptomics studies have shown that more than 25% of transcripts of the identified ethylene synthesis and signaling genes increase significantly during developmental leaf senescence (Jibran et al., 2013). However, ethylene by itself is not necessary or sufficient for the onset of senescence. This is shown by the fact that plants carrying the ethylene-insensitive mutations eventually senesce (Jing et al., 2002). Ethylene-constitutive response and overexpression mutants such as etr and eto in Arabidopsis do not show premature leaf senescence (Gan, 2010; Jing et al., 2002). Premature senescence is also not reported in ethylene-overproducing tomato plants that express the ACC synthase gene (Gan, 2010; Jing et al., 2002). This evidence thus suggests that ethylene does not directly regulate the beginning of senescence, but rather modulates the timing of it (Morris et al., 2000). Thus, ethylene can induce senescence only when the leaf has gone through developmental changes controlled by its age (Jing et al., 2005).
3.3 Salicylic Acid and Senescence SA, also known as mono-hydroxy benzoic acid, is an endogenous signal involved in the regulation of a number of plant development processes (Barman et al., 2016), including cell growth, respiration, transpiration, SAG expression, stomatal closure, and thermogenesis. SA also regulates plant response to abiotic stresses, such as drought, salinity, ultraviolet B (UV-B) irradiation, ozone exposure, and chilling (Barman et al., 2016; Jibran et al., 2013; Zhang et al., 2013). SA is synthesized by two pathways: the phenylalanine ammonia lyase (PAL) pathway and the isochorismate (IC) pathway. Both of these use chorismate as the primary metabolite (Barman et al., 2016; Zhang et al., 2013). Chorismate-derived L-phenylalanine is converted into SA via benzoate intermediates or coumaric acid via a number of enzymatic reactions involving PAL, benzoic acid 2-hydroxylase, and other unknown enzymes. Chorismate also can be converted to SA via IC in a two-step process involving isochorismate synthase (ICS) and isochorismate pyruvate lyase (IPL; Barman et al., 2016; Zhang et al., 2013). The role of SA in age-dependent leaf senescence has been reported on recently. SA is involved in the upregulation of several SAGs, with internal SA concentrations being four times higher in senescing leaves of Arabidopsis. For example, delayed senescence is observed in phytoalexin-deficient 4 (pad4), nonexpresser of pathogen-related genes (npr1), and naphthalene oxygenase (NahG)–expressing Arabidopsis mutants compared with wild-type plants (Morris et al., 2000). The transcriptome changes induced by the SA pathway are very much
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like those mediated by age-dependent senescence. This is further supported by the observation that age-dependent senescence is delayed in NahG-overexpressing mutants that produce very low SA concentrations (Lim et al., 2007). It also has been reported that SA regulates the expression of transcription factors like WRKY53, WRKY54, and WRKY70, which are involved in the regulation of senescence (Thakur et al., 2016; Morris et al., 2000).
3.4 Auxin and Senescence Auxins regulate the synthesis of other hormones, and along with CKs, they control plant growth and development (Thakur et al., 2016). The most commonly active auxins are indole acetic acid (IAA) and indole butyric acid (IBA), and these are synthesized from tryptophan (Trp; Thakur et al., 2016). The site of IAA biosynthesis is primarily in the leaf primordial, young leaves, and developing seeds, with cell-to-cell transport occurring via the vascular cambium, procambial strands, and epidermal cells (Davies, 2010). Trp is the main precursor for IAA biosynthesis in plants via four main pathways. In the YUCCA (YUC) pathway, auxin is produced when Trp is converted to tryptamine. The indole-3-pyruvic acid (IPA) pathway, which converts Trp to indole-3-pyruvic acid, is a major IAA biosynthetic pathway in Arabidopsis. Another pathway found in most plants is the indole-3-acetamide (IAM) pathway, where Trp is converted to IAM. Finally, the indole-3- acetaldoxime (IAOx) pathway, which is active only in plants that have CYP79B family members, converts Trp to IAOx. The involvement of auxin in leaf senescence has been demonstrated in studies utilizing the external application of auxin. Generally, external application of natural and synthetic auxins leads to delayed chlorophyll loss and protein degradation in detached leaves of various plant species. The levels of endogenous auxins were also shown to be reduced at the onset of and during senescence in these leaves. Repression of transcription of some SAGs was also observed when auxin was applied externally (Mueller-Roeber and Balazadeh, 2014). In Mueller-Roeber and Balazadeh (2014), SAG12 was the reference senescence marker and was downregulated in Arabidopsis leaves incubated in 5 μM indole-3-acetic acid (IAA). However, there are conflicting observations regarding the effects of externally applied auxin on leaf senescence (Mueller-Roeber and Balazadeh, 2014). In some cases, the exogenous application of auxin did nothing, whereas in other cases, senescence was accelerated. The exogenous application of high concentrations of auxin is known to facilitate ethylene production, and thus senescence. Recent studies also support this observation by showing that levels of free IAA in Arabidopsis reach concentrations twice as high in half-yellowing leaves than in mature green leaves. Upregulation of nitrilase genes that convert IAN to IAA and other IAA biosynthesis genes (Trp synthase and IAAld oxidase) have been reported during leaf senescence (Gan, 2010).
3.5 Abscisic Acid and Senescence ABA is synthesized from glyceraldehydes-3-phosphate via isopentenyl diphosphate and carotenoids (Chengzhen and Chengcai, 2015; Davies, 2010). This usually occurs in roots and mature leaves. After synthesis, it is transported from the roots via the xylem and the
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phloem if the site of synthesis is the leaves. Inhibition of shoot growth, stomatal closure, and maintenance of seed dormancy are some of the effects of ABA on plant growth and development. Senescence has been induced in detached leaves exogenously treated with ABA. High concentrations of ABA are found in leaves at the beginning of and during senescence, but there is a reduction in ABA concentrations in the later stages (Gan, 2010). Also, during senescence, there is upregulation of some of the ABA-signaling genes and SAGs (Chengzhen and Chengcai, 2015). In Arabidopsis, the gene that codes an important enzyme in ABA biosynthesis, 9-cis-epoxycaretonoid dioxygenase is upregulated during senescence. Also, upregulation of genes coding for ABA-signaling proteins (ABI1 and 2), and ABA-responsive element binding factors is observed in senescing Arabidopsis (Fischer, 2012). Expression of a number of SAGs is induced by exogenously applied ABA, which speeds up the leaf-senescence process (Chengzhen and Chengcai, 2015). Also, a number of biotic and abiotic stresses have been shown to increase ABA concentrations and activate senescence- signaling pathways. This gives an indication that ABA regulates the initiation and progression of leaf senescence (Chengzhen and Chengcai, 2015). However, the specific role of ABA has not been properly elucidated by functional studies of mutants that are deficient in either ABA biosynthesis or perception (Gan, 2010). In Arabidopsis, the ABA-induced receptor protein kinase 1 (RPK1) positively regulates senescence. Senescence is promoted significantly in mutants overexpressing RPK1, while RPK1 knockout mutants have decreased sensitivity to ABA-induced senescence. However, overexpression of RPK1 retarded growth in the mutants but did not result in senescence symptoms, suggesting that the role of RPK1 in ABA-induced leaf senescence depends on the developmental stage (Chengzhen and Chengcai, 2015).
3.6 Gibberellin Acids and Senescence Gibberellin acids (GAs) are a group of more than 125 compounds based on the ent- giberellane structure (Davies, 2010). In plants, GA1 is the most important GA, as it is involved in stem elongation. GA3, a fungal derivative, is the most available compound. Synthesis of GAs starts from glyceraldehyde-3-phosphate via isopentenyl diphosphate. The site of synthesis is usually the tissue of young shoots and developing seeds, and the process starts in the chloroplast in the membrane and cytoplasm (Davies, 2010). GA mediates a number of plant growth and development processes, such as seed germination, flowering, cone production, inhibition of leaf and fruit senescence, and stem elongation. In germinating cereal grains, GA stimulates the production of beta-amylase (Gan, 2010). GA activity and leaf senescence have an inverse relationship that has been reported on in a number of plant species, including lettuce, nasturtium, and dandelion (Fischer, 2012). The external application of GA has been shown to inhibit senescence in many plant species, and this is done by the inhibition of chlorophyll, protein, and nucleic acid degradation in leaves. Some GA species are more effective than others in inhibiting senescence. A good example is GA4, which is twice as active in delaying leaf senescence of Alstroemeria hybrida as GA1. GA4 + 7 also has been shown to inhibit leaf senescence in a number of plants. Free GA (GA4 and GA7) is required to initiate leaf senescence. Leaf senescence was inhibited in Paris polyphylla when GA was exogenously applied. On the other hand, inhibition of
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GA synthesis by paclobutrazol accelerated senescence (Jibran et al., 2013). Therefore, it has been suggested that inhibition of senescence in P. polyphylla by GA was due to antagonizing ABA effects or by preserving sugars due to decreased respiration in Lilium longiflorum (Easter lily; Jibran et al., 2013).
3.7 Cytokinins and Senescence CKs are adenine derivatives that, along with auxin, induce cell division in tissue culture. Zeatin is the most abundant CK base found in plants. CKs also exist as ribosides and ribotides. They are synthesized by biochemical modification of adenine and are transported via the xylem from roots and shoots (Davies, 2010). CKs have been shown to inhibit senescence. Endogenous levels of CK are low during senescence, while external application of CK has been shown to delay the start of senescence in a number of monocotyledon and dicotyledon plants. Yellow leaves have been shown to regreen when exogenously treated with CKs (Gan, 2010). CK synthesis primarily takes place in the roots and are transported to shoots and leaves via the xylem. As a result, concentrations of CK in xylem sap and the stage of senescence are inversely proportional. This was demonstrated in rice, where the xylem sap of Akenohoshi (a late-senescing cultivar) contained more CK than the xylem sap of Nipponbare (a normal- senescing cultivar). CK biosynthesis genes are downregulated, while the activity enzyme CK oxidase is elevated during senescence (Thakur et al., 2016). In Arabidopsis, CK signaling is initiated by AHK2, AHK3, and AHK4, which are histidine protein kinases and also act as CK receptors (Davies, 2010; Zwack et al., 2013). The receptors autophosphorylate and transfer CK signals via histidine phosphor-transfer proteins to nuclear-localized Arabidopsis response regulators (ARRs), which regulate the transcription of CK target genes. AHK3 is also crucial to CK-mediated leaf longevity (Davies, 2010; Zwack et al., 2013). Overexpression of AHK3 delays leaf senescence, while a knockout mutation in AHK3 reduces CK sensitivity (Khan et al., 2014). CK response factor 6 (CRF6) is a transcription factor that has been shown to be involved in the delay of dark-induced senescence. Plants overexpressing CRF6 and crf6 mutants have been found to have reduced sensitivity to the senescence-delaying effects of CK (Zwack et al., 2013).
4 PGR CROSS-TALK The cross-talk among plant hormones is a central theme in many biological processes, including senescence. As mentioned earlier in this chapter, exogenously applied PGRs affect the level and activities of endogenous PGRs, which in turn affect the regulation of other PGRs. Thus, one cannot ignore the fact that the regulatory mechanisms of various PGRs are intertwined and overlap, thus bringing the concept of hormonal cross-talk. In their regulation of senescence, PGRs are involved in three categories of cross-talk, including direct and indirect cross-talk and coregulation (Fig. 1), as outlined by Hoffmann et al. (2011). Interestingly, it has been shown in other studies (Kim et al., 2009; Sharabi-Schwager et al., 2010) that JA-, ethylene-, and ABA-induced leaf senescence were delayed in the knockout plants of EIN2 and ORE9,
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4 PGR Cross-Talk
Stimulus Environmental or developmental
Indirect cross-talk
Direct cross-talk
One stimulus affects one PGR, which affects another PGR, the two PGRs; affect targeted genes to initiate a single response
One stimulus affects two or more PGRs and acts on a defined target gene to initiate a single response
Coregulation One stimulus affects two or more PGRs and acts on a defined target gene to initiate a single response
FIG. 1 Three types of cross-talk that occur in PGRs, as influenced by environmental and developmental stimuli.
which was an indication that these hormonal functions overlap in regulating senescence. Details of the interaction of SA with other PGRs have been outlined by An and Mou (2011). As mentioned previously, GA is a senescence-retarding hormone whose activity declines with the age of the plant; however, it indirectly regulates senescence by acting antagonistically with ABA. While ABA interacts with GA, the exogenous application of ABA increases ethylene production; the same is true for the exogenous application of ethylene. These both form a stronger force to encourage the induction of senescence. Furthermore, ethylene production is stimulated by Br treatments, and Br also stimulates JA biosynthesis, which in turn enhances ethylene production. Although the responses orchestrated by senescence-retarding PGRs and senescence-inhibiting PGRs are clearly different, there are possibilities of cross-talk between these distinct senescence PGRs with exogenous application of ABA-reducing CK, while the same response occurs upon exogenous application of CK (Gan, 2010).
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5 CONCLUSION Taken together, these findings indicate that the application of a particular exogenous PGR not only will affect the counterpart endogenous hormone, but it also will elucidate a series of responses and cross-talks with other PGRs, leading to senescence. Therefore, when studying the effects of PGRs on senescence, it is necessary to focus on the cross-talk among PGRs rather than the sole effect of a single PGR because in plants, no single PGR works in isolation from other PGRs.
Acknowledgments The authors gratefully acknowledge the financial support of 973 National Project (517102-N51501/001), the National Natural Science Foundation of China Project, the International (Regional) Cooperation and Exchange Program (517102-N11808ZJ), the Fundamental Research Funds for the Central Universities (517102*172210172) and the Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP).
References An, C., Mou, Z., 2011. Salicylic acid and its function in plant immunity. J. Integr. Plant Biol. 53 (6), 412–428. Barman, K., Sharma, S., Kumari, P., Siddiqui, M.W., 2016. Salicylic acid. In: Siddiqui, M.W. (Ed.), Postharvest Management Approaches for Maintaining Quality of Fresh Produce. Springer International Publishing, Switzerland, pp. 51–68. https://doi.org/10.1007/978-3-319-23582-0. Besseau, S., Li, J., Palva, E.T., 2012. WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 63, 2667–2679. Buchanan-wollaston, V., Earl, S., Harrison, E., Mathas, E., Navabpour, S., Page, T., 2003. The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnol. J. 1, 3–22. Canakci, S., Dursum, B., 2012. The effect of pre-application of salicylic acid on some physiological and biochemical characteristics of tomato seedling (Lycopersicon esculentum L) growing in cadmium containing media. Afr. J. Biotechnol. 11, 3173–3178. Chengzhen, L., Chengcai, C.H.U., 2015. Towards understanding abscisic acid-mediated leaf senescence. Sci. China Life Sci. 58 (5), 506–508. https://doi.org/10.1007/s11427-015-4846-z. Criado, V.M., Roberts, I.N., Echeverria, M., Barneix, A.J., 2007. Plant growth regulators and induction of leaf senescence in nitrogen-deprived wheat plants. J. Plant Growth Regul. 26, 301–307. https://doi.org/10.1007/ s00344-007-9016-5. Davies, P.J. (Ed.), 2010. Plant Hormones: Biosynthesis, Signal Transduction, Action! third ed. Springer, Netherlands. https://doi.org/10.1007/978-1-4020-2686-7. Fang, C., Zhang, H., Wan, J., Wu, Y., Li, K., Jin, C., Luo, J., 2016. Control of leaf senescence by an MeOH-Jasmonates Cascade that is epigenetically regulated by OsSRT1 in rice. Mol. Plant 9 (10), 1366–1378. https://doi.org/10.1016/j. molp.2016.07.007. Ferrante, A., Francini, A., 2006. Ethylene and leaf senescence. In: Khan, N.A. (Ed.), Ethylene Action in Plants. Springer, Berlin, Heidelberg, pp. 51–67. Fischer, A.M., 2012. The complex regulation of senescence. Crit. Rev. Plant Sci. 31 (2), 124–147. https://doi.org/10.1 080/07352689.2011.616065. Gan, S., 2010. The hormonal regulation of senescence. In: Davies, P.J. (Ed.), Plant Hormones: Biosynthesis, Signal Transduction, Action! third ed. Springer, Netherlands, pp. 597–617. https://doi. org/10.1007/978-1-4020-2686-7. Gan, S., Amasino, R.M., 1997. Making sense of senescence. Plant Physiol. 113, 313–319. He, Y., Fukushige, H., Hildebrand, D.F., Gan, S., 2002. Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol. 128. https://doi.org/10.1104/pp.010843. Himelblau, E., Amasino, M., 2001. Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J. Plant Physiol. 158, 1317–1323.
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Hoffmann, M., Hentrich, M., Pollmann, S., 2011. Auxin-Oxylipin crosstalk. Relationship of antagonists. J. Integr. Plant Biol. 53 (6), 429–445. Hu, Y., Jiang, Y., Han, X., Wang, H., Pan, J., Yu, D., 2017. Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J. Exp. Bot. 68 (6), 1361–1369. Islam, M.M., Ishibashi, Y., Nakagawa, A.C.S., Tomita, Y., Zhao, X., Iwaya-Inoue, M., Arima, S., Zheng, S.H., 2017. Nitrogen manipulation affects leaf senescence during late seed filling in soybean. Acta Physiol. Plant. 39, 42. Jibran, R., Hunter, D.A., Dijkwel, P.P., 2013. Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol. 82, 547–561. https://doi.org/10.1007/s11103-013-0043-2. Jing, H.-C., Sturre, M.J.G., Hille, J., Dijkwel, P.P., 2002. Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J. 32 (1), 51–63. https://doi. org/10.1046/j.1365-313X.2002.01400.x. Jing, H., Schippers, J.H.M., Hille, J., Dijkwel, P.P., 2005. Ethylene-induced leaf senescence depends on age- related changes and OLD genes in Arabidopsis. J. Exp. Bot. 56 (421), 2915–2923. https://doi.org/10.1093/ jxb/eri287. Khan, M., Rozhon, W., Poppenberger, B., 2014. The role of hormones in the aging of plants—a mini-review. Gerontology, 49–55. https://doi.org/10.1159/000354334. Kim, J.H., Woo, H.R., Kim, J., Lim, P.O., Lee, I.C., Choi, S.H., Hwang, D., Nam, H.G., 2009. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323, 1053. Kim, J.H., Chung, K.M., Woo, H.R., 2011. Three positive regulators of leaf senescence in Arabidopsis, ORE1, ORE3 and ORE9, play roles in crosstalk among multiple hormone-mediated senescence pathways. Genes Genom. 33, 373–381. Kim, J., Chang, C., Tucker, M.L., 2015. To grow old : regulatory role of ethylene and jasmonic acid in senescence. Front. Plant Sci. 6, 1–7. https://doi.org/10.3389/fpls.2015.00020. Lim, P.O., Kim, H.J., Nam, H.G., 2007. Leaf senescence. Annu. Rev. Plant Biol. 58. https://doi.org/10.1146/annurev. arplant.57.032905.105316. Masclaux, C., Valadier, M.H., Brugière, N., Morot-Gaudry, J.F., Hirel, B., 2011. Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211, 510. https://doi.org/10.1007/s004250000310. Morris, K., Soheila, A., Page, T., John, C.F., Murphy, A.M., Carr, J.P., Buchanan-wollaston, V., 2000. Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J. 23 (5). Mueller-Roeber, B., Balazadeh, S., 2014. Auxin and its role in plant senescence. J. Plant Growth Regul. 33, 21–33. https://doi.org/10.1007/s00344-013-9398-5. Pandey, S., Ranade, S.A., Nagar, P.K., Kumar, N., 2000. Review role of polyamines and ethylene as modulators of plant senescence. J. Biosci. 25 (3). Sharabi-Schwager, M., Lers, A., Samach, A., Guy, C.L., Porat, R., 2010. Overexpression of the CBF2 transcriptional activator in Arabidopsis delays leaf senescence and extends plant longevity. J. Exp. Bot. 61, 261–273. Shi, Y., Tian, S., Hou, L., Huang, X., Zhang, X., Guo, H., Yang, S., 2012. Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-a ARR genes in Arabidopsis. Plant Cell 24, 2578–2595. Song, Y., Xiang, F., Zhang, G., Miao, Y., Miao, C., Song, C.P., 2016. Abscisic acid as an internal integrator of multiple physiological processes modulates leaf senescence onset in Arabidopsis thaliana. Front. Plant Sci. 7, 181. https:// doi.org/10.3389/fpls.2016.00181. Thakur, N., Sharma, V., Kishore, K., 2016. Leaf senescence : an overview. Indian J. Plant Physiol. 21 (3), 225–238. https://doi.org/10.1007/s40502-016-0234-3. Wu, L., Ma, N., Jia, Y., Zhang, Y., Feng, M., Jiang, C.Z., Ma, C., Gao, J., 2017. An ethylene-induced regulatory module delays flower senescence by regulating Cytokinin content. Plant Physiol. 173 (1), 853–862. https://doi. org/10.1104/pp.16.01064. Yoshida, S., 2003. Molecular regulation of leaf senescence. Curr. Opin. Plant Biol. 6, 79–84. Zhang, K., Halitschke, R., Yin, C., Liu, C., Gan, S., 2013. Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. PNAS 110 (36), 14807–14812. https://doi.org/10.1073/ pnas.1302702110. Zwack, P.J., Robinson, B.R., Risley, M.G., Rashotte, A.M., 2013. Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to Cytokinin and numerous abiotic stresses. Plant Cell Physiol. 54 (6), 971–981. https://doi.org/10.1093/pcp/pct049.
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Further Reading Guiboileau, A., Sormani, R., Meyer, C., Masclaux-Daubresse, C., 2010. Senescence and death of plant organs: Nutrient recycling and developmental regulation. C. R. Biol. 333, 382–391. Noodén, L.D., Guiamét, J.J., John, I., 2004. Whole plant senescence. In: Plant Cell Death Processes, pp. 227–244. https://doi.org/10.1016/B978-012520915-1/50018-7. Woo, H.R., Kim, H.J., Nam, H.G., Lim, P.O., 2013. Plant leaf senescence and death—regulation by multiple layers of control and implications for aging in general. J. Cell Sci. 126, 4823–4833.
6 The Role of Growth Regulators in Senescence Imran Haider Shamsi⁎, Tichaona Sagonda⁎, Xin Zhang†, Gerald Zvobgo⁎, Heren Issaka Joan⁎ ⁎
Department of Agronomy, Institute of Crop Science, Zhejiang University, Hangzhou, People’s Republic of China †School of Marxism, Zhejiang University, Hangzhou, People’s Republic of China
1 INTRODUCTION The final stage of leaf development, termed senescence, includes programmed cell death (PCD). The timing and occurrence of senescence in plant species and genotypes are influenced by a number of factors. Because developmental senescence is initiated regardless of the normal growth of the plant, it is possible that the process is genetically programmed. Thus, the process of senescence can be described further as genetically programmed cell death (PCD) that is extensively controlled by multiple layers of regulation, including translational and posttranslational regulation (Gan and Amasino, 1997). Senescence occurs in specific organs or in the organism as a whole, with grains like rice and wheat exhibiting its effects during their harvest periods, in contrast, the leaves of deciduous trees change from green to yellow in autumn, an indication of organ-specific senescence (Yoshida, 2003). Leaf senescence is required for plant survival because as old leaves degrade, their products are translocated to young leaves, which will serve as nutrients (Himelblau and Amasino, 2001). Due to the complexity and orderliness of events in senescence, it is clear that the process is not controlled by a single factor, but rather by several factors, including low nitrogen (Islam et al., 2017), high sugar content (Masclaux et al., 2011), cold stress, salinity stress, and plant growth regulators (PGRs).
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2 PLANT GROWTH REGULATORS The term PGR has been widely used to describe any substance that can be used to regulate the growth of a whole plant or a specific part of a plant, regardless of the source of production. However, a clear distinction needs to be made between plant hormones and exogenously produced PGRs. Plant hormones are naturally produced signal molecules that operate under minute concentrations, while PGRs are synthetic chemicals used to alter the growth of plants. The most common naturally produced hormones include abscisic acid (ABA), jasmonic acid (JA), salicylic acid (SA), cytokinins (CKs), auxin, gibberellic acid (GA), and ethylene. PGRs act as natural plant hormones, with their biological activity similar to or exceeding that of the equivalent endogenous hormones. Apart from natural plant hormones, other natural growth substances exist, such as brassinosteroids (BRs), oligosaccharides, systenins, polyamines, phosphoinositosides, and SA, all of which are responsible for altering the growth of plants via a number of mechanisms. Natural growth substances, along with PGRs, may alter the synthesis, destruction, activation, and sensitivity to the equivalent natural plant hormones or other types. Thus, in this chapter, we will use the term PGR to refer to any chemical that stimulates or inhibits plant growth, regardless of its site of production. Due to the complexity of the regulation process, PGRs function by themselves or in combination with other classes of PGRs, whether simultaneously or sequentially. In addition to inducing senescence, PGRs alter the formation of flowers and leaves and initiate fruit ripening. The function and interaction of PGRs with various transcriptional factors and their cross-talk among each other stand out, principally due to their roles in plant senescence. Thus, it is imperative to outline the importance of and the regulatory mechanism of PGRs in senescence.
3 PGRS IN SENESCENCE The role of senescence is to facilitate the remobilization of nutrients from moribund parts to actively growing parts. PGRs utilize both environmental and developmental cues to enable senescence to acclimatize the plant to a wide range of environmental conditions so as to extract the maximum amount of nutrients from the moribund tissues. Because of their varying structures, PGRs play a number of possible roles in plant senescence, with some such as ABA, JA, and SA inducing senescence, while CK, auxin, and GA elucidate a contrasting response. Over the past decade, in-depth studies have been done on the functions of PGRs in regulating senescence, including auxin, ethylene (Wu et al., 2017), JA (He et al., 2002), ABA (Song et al., 2016), and SA. In addition, various studies have outlined the cross-talk among various PGRs (Kim et al., 2011; Hu et al., 2017) while regulating plant senescence, and all of the findings agree on the functions of PGRs in senescence. PGRs regulate senescence in multiple ways, with some not directly involved in the regulation of senescence, but rather working antagonistically with other PGRs (Jibran et al., 2013), while others regulate the progression rather than the onset of senescence. In addition, some defense-related PGRs, like SA, JA, and ethylene, tend to accumulate more in the final stages of leaf senescence due to their role in protecting plants from biotic stress because older leaves are more prone to the vagaries of biotic stress.
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The underlying question would be about how PGRs modulate senescence. PGRs are very important in plant development and adaptation to stress, and thus they are crucial in senescence because senescence is a developmentally regulated process modulated by stress (Jibran et al., 2013). PGRs influence leaf senescence in all the plant development stages—that is, by affecting leaf developmental stages, influencing environmental signals, and regulating the speed of senescence once the leaf has initiated the process (Jibran et al., 2013). They are responsible for signal regulation of stress-related genes, senescence-associated genes (SAGs), and transcription factors that are essential for plant survival and growth. The WRKY family of transcription factors stands out as an important group of substances that PGRs regulate in senescence. The PGRs regulate the WRKY in a series of events that has been proposed by Besseau et al. (2012), including the expression of negative regulators before leaf senescence, and then they simultaneously induce positive and negative regulators at the beginning of senescence following positive regulation during the senescence. Studies in knockout mutant and overexpressing lines have shown inhibition or enhanced cell death in natural environments upon the exogenous application of PGRs. Furthermore, under stressful conditions, exogenous application of other PGRs has been shown to reduce a plant’s tolerance to abiotic stress (Shi et al., 2012), while other PGRs like SA increase this tolerance (Canakci and Dursum, 2012). PGRs function in acclimatization to various abiotic stresses by regulating the sensitivity and responsiveness of tissues. It is also noteworthy that the process of senescence is induced at a certain developmental stage, and thus the effects of some of the PGRs also depend on leaf maturity, with the supply in mature leaves inducing the onset of senescence, while the same does not occur in young leaves (Jing et al., 2002). Taken together, one can postulate that PGRs like auxins and BRs are modulators of plant development, while JA, SA, and BA respond to stress and other environmental signals. Thus it is clear that the role of each PGR needs to be elucidated to understand its precise role in senescence. Therefore, this chapter will give an outline of the regulation of senescence, focusing on the commonly known PGRs, their functions, current findings, and their crosstalk with each other. Although many studies have focused on individual PGRs, it is important to note that PGRs communicate with each other in regulating senescence, with some working to antagonistic effect and others cooperating with each other. Due to overlapping of PGRs in their mode of action, the regulation of senescence by PGRs is a complex mechanism that needs deeper understanding.
3.1 Jasmonic Acid and Senescence Jasmonates are derived from beta-linolenic acid, and they regulate various plant growth and development stages, such as fertility, anthocyanin production, root growth, seed germination, senescence, and plant defense mechanisms against biotic and abiotic stress (Kim et al., 2015; Jibran et al., 2013). JA was first reported as a hormone when methyl jasmonate (MeJA) was shown to induce senescence in wormwood and detached oat (Avena sativa) leaves (Kim et al., 2015; Gan, 2010; He et al., 2002). The biosynthesis of JA is catalyzed by several enzymes, such as allene oxide synthases (AOSs), allene oxide cyclases (AOCs), 12-oxo-phytodienoic acid (OPDA) reductases (OPRs), and acyl-CoA oxidases (ACXs) (Fang et al., 2016). JA carboxy methyl transferases (JMTs) and jasmonoyl isoleucine conjugate synthases (JARs) are included in the generation
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of bioactive forms, MeJA, and jasmonate-isoleucine (JA-Ile; Fang et al., 2016). Two main pathways exist for JA biosynthesis, with one localized in the chloroplast and the other localized in the cytoplasm; and both have alpha-linolenic acid as the first compound in the JA biosynthetic pathway. Evidence of the pathway localized in the cytoplasm is provided by a functional study involving overexpression of a cytosolic AOS in tobacco (Nicotiana tabacum) (He et al., 2002). Recent studies in Arabidopsis show that JA is involved in leaf senescence, and this is demonstrated by mutation studies of the JA synthesis and receptor genes, as well as studies measuring plant responses to JA and its many derivatives. For example, temporal shifts in the start of natural and dark-induced senescence have been observed in Arabidopsis plants, with mutations that result in reduced JA levels and make the mutants insensitive to JA (Kim et al., 2015). Early onset of senescence in attached and detached leaves also has been observed in wild-type Arabidopsis treated with exogenous JA at 30 μM, but the same treatment fails to induce senescence in JA-insensitive mutants. This seems to indicate that the JA-signaling pathway is required in order for JA to promote leaf senescence (Gan, 2010). JA biosynthesis genes have been reported to be differentially expressed during leaf senescence, with JA concentrations four times higher in senescing leaves than in nonsenescing leaves (Gan, 2010; Kim et al., 2015; Criado et al., 2007). A number of studies have concluded that synthesis of JA during leaf senescence could be a secondary by-product from the breakdown of macromolecules and membranes in the process of senescence (Kim et al., 2015). However, contradicting results have been reported regarding the role of JA in dark-induced senescence from studies looking at a range of mutants in JA biosynthesis and signaling (Jibran et al., 2013). Delayed dark-induced leaf senescence has been shown in JA-signaling-impaired mutants (such as coil-2) and reduced jasmonate content mutants via silencing of the beta- oxidation gene 3-Ketoacyl-CoA Thiolase-2 (KAT2). However, delayed dark-induced senescence is not observed in other mutants, such as AOS and oxophytodienoic acid reductase (OPR3; Jibran et al., 2013).
3.2 Ethylene and Senescence Ethylene is an important phytohormone that affects a number of plant development processes, including fruit ripening, cell division, abiotic and biotic stress response, cell elongation, and senescence. For example, mutant plants, in which ethylene signaling is overexpressed, show higher survival rates under salt stress when compared to wild-type plants (Jibran et al., 2013). Also, overexpression of the ethylene-inducible transcription factor AtEBP in tobacco stops cell death caused by exposure to hydrogen peroxide (H2O2), and heat (Jibran et al., 2013). Ethylene production is also increased in response to water stress, mechanical wounding, and biotic stresses (Pandey et al., 2000). Ethylene is synthesized from methionine via a pathway involving the conversion of S-adenosylmethionine (SAM) to a cyclic amino acid, 1-amino cyclo propane-1-carboxylic acid (ACC) catalyzed by ACC synthase, with the intermediate being converted to ethylene by oxidation of ACC oxidase (Pandey et al., 2000). The senescence-promoting properties of ethylene were first observed in leaves and stems exogenously treated with ethylene (Ferrante and Francini, 2006). These experiments showed that ethylene treatment induced typical leaf senescence symptoms, including chlorophyll,
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protein, and macromolecule degradation, as well as an increase in catabolic enzymatic activity (Gan, 2010). However, leaf maturity determines the extent to which ethylene can speed up the senescence of leaves. Ethylene in mature leaves leads to an early start of senescence, while it does not do so in young leaves (Jibran et al., 2013). The regulatory mechanism of ethylene during senescence was unknown until recent studies in Arabidopsis shed much needed light (Kim et al., 2015). Delayed senescence was observed in the leaves of an ethylene- insensitive mutant of Arabidopsis (Etr1). The etr1-1 mutation inhibits the receptor from binding ethylene, making the mutants insensitive to ethylene (Gan, 2010). This experiment lends support to the promoter role of ethylene in senescence. In addition, certain Arabidopsis mutant lines with ethylene signaling-defective genes (ein2), which renders the mutants insensitive to ethylene, showed delayed senescence (Buchanan-wollaston et al., 2003; Gan, 2010). Other transcriptomics studies have shown that more than 25% of transcripts of the identified ethylene synthesis and signaling genes increase significantly during developmental leaf senescence (Jibran et al., 2013). However, ethylene by itself is not necessary or sufficient for the onset of senescence. This is shown by the fact that plants carrying the ethylene-insensitive mutations eventually senesce (Jing et al., 2002). Ethylene-constitutive response and overexpression mutants such as etr and eto in Arabidopsis do not show premature leaf senescence (Gan, 2010; Jing et al., 2002). Premature senescence is also not reported in ethylene-overproducing tomato plants that express the ACC synthase gene (Gan, 2010; Jing et al., 2002). This evidence thus suggests that ethylene does not directly regulate the beginning of senescence, but rather modulates the timing of it (Morris et al., 2000). Thus, ethylene can induce senescence only when the leaf has gone through developmental changes controlled by its age (Jing et al., 2005).
3.3 Salicylic Acid and Senescence SA, also known as mono-hydroxy benzoic acid, is an endogenous signal involved in the regulation of a number of plant development processes (Barman et al., 2016), including cell growth, respiration, transpiration, SAG expression, stomatal closure, and thermogenesis. SA also regulates plant response to abiotic stresses, such as drought, salinity, ultraviolet B (UV-B) irradiation, ozone exposure, and chilling (Barman et al., 2016; Jibran et al., 2013; Zhang et al., 2013). SA is synthesized by two pathways: the phenylalanine ammonia lyase (PAL) pathway and the isochorismate (IC) pathway. Both of these use chorismate as the primary metabolite (Barman et al., 2016; Zhang et al., 2013). Chorismate-derived L-phenylalanine is converted into SA via benzoate intermediates or coumaric acid via a number of enzymatic reactions involving PAL, benzoic acid 2-hydroxylase, and other unknown enzymes. Chorismate also can be converted to SA via IC in a two-step process involving isochorismate synthase (ICS) and isochorismate pyruvate lyase (IPL; Barman et al., 2016; Zhang et al., 2013). The role of SA in age-dependent leaf senescence has been reported on recently. SA is involved in the upregulation of several SAGs, with internal SA concentrations being four times higher in senescing leaves of Arabidopsis. For example, delayed senescence is observed in phytoalexin-deficient 4 (pad4), nonexpresser of pathogen-related genes (npr1), and naphthalene oxygenase (NahG)–expressing Arabidopsis mutants compared with wild-type plants (Morris et al., 2000). The transcriptome changes induced by the SA pathway are very much
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like those mediated by age-dependent senescence. This is further supported by the observation that age-dependent senescence is delayed in NahG-overexpressing mutants that produce very low SA concentrations (Lim et al., 2007). It also has been reported that SA regulates the expression of transcription factors like WRKY53, WRKY54, and WRKY70, which are involved in the regulation of senescence (Thakur et al., 2016; Morris et al., 2000).
3.4 Auxin and Senescence Auxins regulate the synthesis of other hormones, and along with CKs, they control plant growth and development (Thakur et al., 2016). The most commonly active auxins are indole acetic acid (IAA) and indole butyric acid (IBA), and these are synthesized from tryptophan (Trp; Thakur et al., 2016). The site of IAA biosynthesis is primarily in the leaf primordial, young leaves, and developing seeds, with cell-to-cell transport occurring via the vascular cambium, procambial strands, and epidermal cells (Davies, 2010). Trp is the main precursor for IAA biosynthesis in plants via four main pathways. In the YUCCA (YUC) pathway, auxin is produced when Trp is converted to tryptamine. The indole-3-pyruvic acid (IPA) pathway, which converts Trp to indole-3-pyruvic acid, is a major IAA biosynthetic pathway in Arabidopsis. Another pathway found in most plants is the indole-3-acetamide (IAM) pathway, where Trp is converted to IAM. Finally, the indole-3- acetaldoxime (IAOx) pathway, which is active only in plants that have CYP79B family members, converts Trp to IAOx. The involvement of auxin in leaf senescence has been demonstrated in studies utilizing the external application of auxin. Generally, external application of natural and synthetic auxins leads to delayed chlorophyll loss and protein degradation in detached leaves of various plant species. The levels of endogenous auxins were also shown to be reduced at the onset of and during senescence in these leaves. Repression of transcription of some SAGs was also observed when auxin was applied externally (Mueller-Roeber and Balazadeh, 2014). In Mueller-Roeber and Balazadeh (2014), SAG12 was the reference senescence marker and was downregulated in Arabidopsis leaves incubated in 5 μM indole-3-acetic acid (IAA). However, there are conflicting observations regarding the effects of externally applied auxin on leaf senescence (Mueller-Roeber and Balazadeh, 2014). In some cases, the exogenous application of auxin did nothing, whereas in other cases, senescence was accelerated. The exogenous application of high concentrations of auxin is known to facilitate ethylene production, and thus senescence. Recent studies also support this observation by showing that levels of free IAA in Arabidopsis reach concentrations twice as high in half-yellowing leaves than in mature green leaves. Upregulation of nitrilase genes that convert IAN to IAA and other IAA biosynthesis genes (Trp synthase and IAAld oxidase) have been reported during leaf senescence (Gan, 2010).
3.5 Abscisic Acid and Senescence ABA is synthesized from glyceraldehydes-3-phosphate via isopentenyl diphosphate and carotenoids (Chengzhen and Chengcai, 2015; Davies, 2010). This usually occurs in roots and mature leaves. After synthesis, it is transported from the roots via the xylem and the
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phloem if the site of synthesis is the leaves. Inhibition of shoot growth, stomatal closure, and maintenance of seed dormancy are some of the effects of ABA on plant growth and development. Senescence has been induced in detached leaves exogenously treated with ABA. High concentrations of ABA are found in leaves at the beginning of and during senescence, but there is a reduction in ABA concentrations in the later stages (Gan, 2010). Also, during senescence, there is upregulation of some of the ABA-signaling genes and SAGs (Chengzhen and Chengcai, 2015). In Arabidopsis, the gene that codes an important enzyme in ABA biosynthesis, 9-cis-epoxycaretonoid dioxygenase is upregulated during senescence. Also, upregulation of genes coding for ABA-signaling proteins (ABI1 and 2), and ABA-responsive element binding factors is observed in senescing Arabidopsis (Fischer, 2012). Expression of a number of SAGs is induced by exogenously applied ABA, which speeds up the leaf-senescence process (Chengzhen and Chengcai, 2015). Also, a number of biotic and abiotic stresses have been shown to increase ABA concentrations and activate senescence- signaling pathways. This gives an indication that ABA regulates the initiation and progression of leaf senescence (Chengzhen and Chengcai, 2015). However, the specific role of ABA has not been properly elucidated by functional studies of mutants that are deficient in either ABA biosynthesis or perception (Gan, 2010). In Arabidopsis, the ABA-induced receptor protein kinase 1 (RPK1) positively regulates senescence. Senescence is promoted significantly in mutants overexpressing RPK1, while RPK1 knockout mutants have decreased sensitivity to ABA-induced senescence. However, overexpression of RPK1 retarded growth in the mutants but did not result in senescence symptoms, suggesting that the role of RPK1 in ABA-induced leaf senescence depends on the developmental stage (Chengzhen and Chengcai, 2015).
3.6 Gibberellin Acids and Senescence Gibberellin acids (GAs) are a group of more than 125 compounds based on the ent- giberellane structure (Davies, 2010). In plants, GA1 is the most important GA, as it is involved in stem elongation. GA3, a fungal derivative, is the most available compound. Synthesis of GAs starts from glyceraldehyde-3-phosphate via isopentenyl diphosphate. The site of synthesis is usually the tissue of young shoots and developing seeds, and the process starts in the chloroplast in the membrane and cytoplasm (Davies, 2010). GA mediates a number of plant growth and development processes, such as seed germination, flowering, cone production, inhibition of leaf and fruit senescence, and stem elongation. In germinating cereal grains, GA stimulates the production of beta-amylase (Gan, 2010). GA activity and leaf senescence have an inverse relationship that has been reported on in a number of plant species, including lettuce, nasturtium, and dandelion (Fischer, 2012). The external application of GA has been shown to inhibit senescence in many plant species, and this is done by the inhibition of chlorophyll, protein, and nucleic acid degradation in leaves. Some GA species are more effective than others in inhibiting senescence. A good example is GA4, which is twice as active in delaying leaf senescence of Alstroemeria hybrida as GA1. GA4 + 7 also has been shown to inhibit leaf senescence in a number of plants. Free GA (GA4 and GA7) is required to initiate leaf senescence. Leaf senescence was inhibited in Paris polyphylla when GA was exogenously applied. On the other hand, inhibition of
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GA synthesis by paclobutrazol accelerated senescence (Jibran et al., 2013). Therefore, it has been suggested that inhibition of senescence in P. polyphylla by GA was due to antagonizing ABA effects or by preserving sugars due to decreased respiration in Lilium longiflorum (Easter lily; Jibran et al., 2013).
3.7 Cytokinins and Senescence CKs are adenine derivatives that, along with auxin, induce cell division in tissue culture. Zeatin is the most abundant CK base found in plants. CKs also exist as ribosides and ribotides. They are synthesized by biochemical modification of adenine and are transported via the xylem from roots and shoots (Davies, 2010). CKs have been shown to inhibit senescence. Endogenous levels of CK are low during senescence, while external application of CK has been shown to delay the start of senescence in a number of monocotyledon and dicotyledon plants. Yellow leaves have been shown to regreen when exogenously treated with CKs (Gan, 2010). CK synthesis primarily takes place in the roots and are transported to shoots and leaves via the xylem. As a result, concentrations of CK in xylem sap and the stage of senescence are inversely proportional. This was demonstrated in rice, where the xylem sap of Akenohoshi (a late-senescing cultivar) contained more CK than the xylem sap of Nipponbare (a normal- senescing cultivar). CK biosynthesis genes are downregulated, while the activity enzyme CK oxidase is elevated during senescence (Thakur et al., 2016). In Arabidopsis, CK signaling is initiated by AHK2, AHK3, and AHK4, which are histidine protein kinases and also act as CK receptors (Davies, 2010; Zwack et al., 2013). The receptors autophosphorylate and transfer CK signals via histidine phosphor-transfer proteins to nuclear-localized Arabidopsis response regulators (ARRs), which regulate the transcription of CK target genes. AHK3 is also crucial to CK-mediated leaf longevity (Davies, 2010; Zwack et al., 2013). Overexpression of AHK3 delays leaf senescence, while a knockout mutation in AHK3 reduces CK sensitivity (Khan et al., 2014). CK response factor 6 (CRF6) is a transcription factor that has been shown to be involved in the delay of dark-induced senescence. Plants overexpressing CRF6 and crf6 mutants have been found to have reduced sensitivity to the senescence-delaying effects of CK (Zwack et al., 2013).
4 PGR CROSS-TALK The cross-talk among plant hormones is a central theme in many biological processes, including senescence. As mentioned earlier in this chapter, exogenously applied PGRs affect the level and activities of endogenous PGRs, which in turn affect the regulation of other PGRs. Thus, one cannot ignore the fact that the regulatory mechanisms of various PGRs are intertwined and overlap, thus bringing the concept of hormonal cross-talk. In their regulation of senescence, PGRs are involved in three categories of cross-talk, including direct and indirect cross-talk and coregulation (Fig. 1), as outlined by Hoffmann et al. (2011). Interestingly, it has been shown in other studies (Kim et al., 2009; Sharabi-Schwager et al., 2010) that JA-, ethylene-, and ABA-induced leaf senescence were delayed in the knockout plants of EIN2 and ORE9,
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4 PGR Cross-Talk
Stimulus Environmental or developmental
Indirect cross-talk
Direct cross-talk
One stimulus affects one PGR, which affects another PGR, the two PGRs; affect targeted genes to initiate a single response
One stimulus affects two or more PGRs and acts on a defined target gene to initiate a single response
Coregulation One stimulus affects two or more PGRs and acts on a defined target gene to initiate a single response
FIG. 1 Three types of cross-talk that occur in PGRs, as influenced by environmental and developmental stimuli.
which was an indication that these hormonal functions overlap in regulating senescence. Details of the interaction of SA with other PGRs have been outlined by An and Mou (2011). As mentioned previously, GA is a senescence-retarding hormone whose activity declines with the age of the plant; however, it indirectly regulates senescence by acting antagonistically with ABA. While ABA interacts with GA, the exogenous application of ABA increases ethylene production; the same is true for the exogenous application of ethylene. These both form a stronger force to encourage the induction of senescence. Furthermore, ethylene production is stimulated by Br treatments, and Br also stimulates JA biosynthesis, which in turn enhances ethylene production. Although the responses orchestrated by senescence-retarding PGRs and senescence-inhibiting PGRs are clearly different, there are possibilities of cross-talk between these distinct senescence PGRs with exogenous application of ABA-reducing CK, while the same response occurs upon exogenous application of CK (Gan, 2010).
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5 CONCLUSION Taken together, these findings indicate that the application of a particular exogenous PGR not only will affect the counterpart endogenous hormone, but it also will elucidate a series of responses and cross-talks with other PGRs, leading to senescence. Therefore, when studying the effects of PGRs on senescence, it is necessary to focus on the cross-talk among PGRs rather than the sole effect of a single PGR because in plants, no single PGR works in isolation from other PGRs.
Acknowledgments The authors gratefully acknowledge the financial support of 973 National Project (517102-N51501/001), the National Natural Science Foundation of China Project, the International (Regional) Cooperation and Exchange Program (517102-N11808ZJ), the Fundamental Research Funds for the Central Universities (517102*172210172) and the Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP).
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Further Reading Guiboileau, A., Sormani, R., Meyer, C., Masclaux-Daubresse, C., 2010. Senescence and death of plant organs: Nutrient recycling and developmental regulation. C. R. Biol. 333, 382–391. Noodén, L.D., Guiamét, J.J., John, I., 2004. Whole plant senescence. In: Plant Cell Death Processes, pp. 227–244. https://doi.org/10.1016/B978-012520915-1/50018-7. Woo, H.R., Kim, H.J., Nam, H.G., Lim, P.O., 2013. Plant leaf senescence and death—regulation by multiple layers of control and implications for aging in general. J. Cell Sci. 126, 4823–4833.