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Li, Z.; Zhao, T.; Liu, J.; Li, H.; Liu, B. Phytohormone-Mediated Leaf Senescence under Shade Conditions. Encyclopedia. Available online: https://encyclopedia.pub/entry/43348 (accessed on 20 July 2025).
Li Z, Zhao T, Liu J, Li H, Liu B. Phytohormone-Mediated Leaf Senescence under Shade Conditions. Encyclopedia. Available at: https://encyclopedia.pub/entry/43348. Accessed July 20, 2025.
Li, Zhuang, Tao Zhao, Jun Liu, Hongyu Li, Bin Liu. "Phytohormone-Mediated Leaf Senescence under Shade Conditions" Encyclopedia, https://encyclopedia.pub/entry/43348 (accessed July 20, 2025).
Li, Z., Zhao, T., Liu, J., Li, H., & Liu, B. (2023, April 23). Phytohormone-Mediated Leaf Senescence under Shade Conditions. In Encyclopedia. https://encyclopedia.pub/entry/43348
Li, Zhuang, et al. "Phytohormone-Mediated Leaf Senescence under Shade Conditions." Encyclopedia. Web. 23 April, 2023.
Phytohormone-Mediated Leaf Senescence under Shade Conditions
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This entry is adapted from the peer-reviewed paper 10.3390/plants12071550

Phytohormones have long been known to affect the onset and progression of leaf senescence, such as ethylene, jasmonic acid (JA), brassinosteroids (BRs), abscisic acid (ABA), and salicylic acid (SA) accelerate leaf senescence. However, auxin and cytokinins (CKs) delay leaf senescence. The content of phytohormones changes drastically in response to the proximity of neighbors, which triggers plant growth adjustments, including enhanced elongation of stems and petioles that enable plants to outgrow their competitors and reach the light and accelerate leaf senescence to escape from the adverse circumstances.

shade light photoreceptor phytohormone leaf senescence

1. Ethylene

Ethylene is a vital gaseous phytohormone that plays crucial roles in multiple biological processes, such as seed germination, fruit ripening, and response to biotic and abiotic stresses [1][2]. The regulatory function of ethylene on leaf senescence is well studied. The ethylene biosynthesis genes are upregulated in senescent leaves, accompanied by an increase in ethylene level [3]. Ethylene treatment accelerates leaf and flower senescence, and inhibition of ethylene biosynthesis and signaling could delay senescence [4][5][6]. However, ethylene cannot directly initiate leaf senescence but is a mediator with its downstream ethylene-responsive factors [6][7]. The volatile phytohormone ethylene has long been associated with shade avoidance response. Ethylene not only functions as a neighbor detection signal via atmospheric accumulation but also as a downstream target of photoreceptors in response to vegetation canopy [8][9][10]. Low R:FR treatment induces a consistent upregulation of ESR2 expression, a marker gene for ethylene signaling that encodes an ethylene receptor protein [11], thus increasing ethylene levels. However, low blue light exposure did not affect ethylene production and the transcription of the ethylene marker gene ERS2 [8]. Ethylene production reduces in the pif4 mutant, and PIF5 could directly regulate the transcription of the master transcription factor of ethylene signaling, indicating that the biosynthesis and signaling of ethylene under the regulation of phyB–PIF pathway [12][13]. Furthermore, ethylene delays the GA-induced degradation of DELLA proteins [14], indicating the crosstalk between phytohormone and light signaling pathway to modulate leaf senescence in response to shading. In Arabidopsis, the mir164 mutant displays premature leaf senescence. The expression of microRNA miR164 decreases with increasing leaf age in an ethylene-dependent manner. Through cleavage of ORE1 mRNA, miR164 represses ORE1 expression [15], indicating that ethylene is involved in microRNA-mediated leaf senescence.

2. Abscisic Acid (ABA)

Abscisic acid (ABA) plays a crucial role in seed germination, seedling development, stomatal movements, and leaf senescence, especially under adverse conditions, thus known as the “stress hormone” [16]. Exogenous application of ABA promotes leaf senescence, and ABA content increases in the senescent leaves of rice, maize, and Arabidopsis [17][18]. ABA promotes leaf senescence by enhancing ethylene production. Furthermore, ABA also activates sucrose nonfermenting 1-related protein kinase 2s (SnRK2s), which subsequently phosphorylates ABA-responsive element-binding factors (ABFs) and related to ABA-insensitive 3/VP1 (RAV1) transcription factors. The phosphorylated ABFs and RAV1 further upregulate the expression of senescence-associated genes (SAGs) and promote leaf senescence in an ethylene-independent manner [19][20]. ABA content increased under shade conditions in sunflower (Helianthus annuus) and tomato leaves [21][22]. Shade elevates the endogenous ABA level, probably by enhancing the transcription levels of ABA biosynthetic genes, such as nine-cisepoxycarotenoid dioxygenase 3 (NCED3) and NCED5 [23]. Several ABA signaling genes, such as ABF3, are also upregulated in response to neighbor proximity [24].

3. Brassinosteroids (BRs)

Brassinosteroids regulate various plant growth and development processes, such as photomorphogenesis, seed germination, floral transition, and responses to biotic and abiotic stresses [25]. BR treatment accelerates senescence, and BR-deficient mutants delay the process of leaf senescence [26][27]. Exogenous treatment of epibrassinolide (eBL) altered leaf senescence in a dosage-dependent manner, with low eBL concentrations retarding leaf senescence and high concentrations accelerating this progression of detached wheat leaves [26]. The BR insensitive1 (bri1) mutants show a prolonged life span concomitant with a decrease in the expression levels of SAGs. Furthermore, bri1-EMS-suppressor 1(BES1) displays accelerated senescence due to the constitutively active BR response [27]. Overexpressing of UGT73C6, a gene encoding a UDP-glycosyltransferase that inactivates BRs, delays leaf senescence in Arabidopsis [28]. Short-term (4 h) simulated shade conditions lead to lower levels of active BR. However, longer period (24 h) conditions abolish the differences in BR levels, suggesting shade-induced BR levels in a dynamic fashion [29]. Under a vegetational canopy, the low R:FR promotes the nuclear accumulation of phyA. The activated phyA reduced COP1 nuclear speckle, leading to changes in downstream target genes, such as PIFs and HY5. These targets regulate the BR signaling pathway by altering the expression of BR biosynthesis genes and protein stability of BES1/BZR1 to influence leaf senescence [30]. Interestingly, DELLAs negatively regulate BR signaling by interacting with BZR1 and reducing the transcription of BR-responsive genes [31]. Furthermore, the transcription factor BZR1 physically interacts with each other and synergistically regulates target genes [32].

4. Strigolactones (SLs)

Strigolactone is a key phytohormone that regulates various physiological processes such as shoot branching, root development, drought tolerance, and leaf senescence [33]. The strigolactone biosynthesis genes more axially growth 3 (MAX3) and MAX4 were drastically elevated during dark incubation, an extreme shade condition [13]. The transcription level of branched 1 (BRC1), the master repressor of branching, is upregulated under shade conditions [34][35]. BRC1 directly binds to and positively regulates the expression of three HD-ZIP protein-encoding genes, which in turn, together with BRC1, enhance the transcription of ABA biosynthesis gene NCED3, leading to the accumulation of ABA and accelerated leaf senescence. Furthermore, under low R:FR conditions, the accumulated PIFs also enhanced the expression of BRC1 and NCED3 [36]. Interestingly, exogenous treatment of ethylene and strigolactone simultaneously could markedly accelerate the process of leaf senescence but not by strigolactone only, demonstrating that strigolactone promotes leaf senescence by enhancing the action of ethylene. These results suggest that different phytohormones cowork and interact with each other to regulate leaf senescence in response to shade conditions.

5. Growth-Promoting Phytohormones Auxin and Gibberellin

Auxin functions in various aspects of cell growth and development [37]. Auxin is known as a negatively acting factor of leaf senescence. Exogenous treatment of auxin inhibits the transcription of SAGs leaf senescence [38]. The expression of IAA biosynthetic genes tryptophan synthase (TSA1), IAAld oxidase (AO1), and nitrilases (NIT1-3) are upregulated in an age-dependent manner. Consequently, the auxin level is elevated during leaf senescence [3]. Studies on the genetic mutation in the auxin signaling pathway further support the involvement of auxin in modulating leaf senescence. Overexpressing of YUCC6 or gain-of-function mutation YUCC6, a gene encoding a flavin-containing monooxygenase that catalyzes the rate-limiting step in the auxin biosynthesis, delay leaf senescence [38]. Disruption of ARF2, a transcription repressor in the auxin signaling pathway, causes a delay in leaf senescence. The reduced ARF2 function releases the repression of auxin signaling with enhanced auxin sensitivity, leading to delayed leaf senescence [39].
Gibberellin is well known for its function in regulating cell elongation, seed germination, dormancy, and floral transition [40][41]. The role of gibberellins in leaf senescence has been elusive on account of their involvement in multiple aspects of plant development processes. GA3 (a bioactive form of gibberellins) treatment retards the process of leaf senescence, leading to increased rhizome yield [42]. Exogenous application GA represses leaf senescence, whereas paclobutrazol, an inhibitor of GA biosynthesis, accelerates the process in paris polyphylla [43][44]. It is possible that gibberellins are not involved in the regulation of leaf senescence directly but, rather, function by antagonizing the effects of ABA. However, exogenous GA3 treatment was shown to induce the expression of WRKY45, a positive regulator of leaf senescence, thus leading to premature leaf senescence [45]. It has been suggested that the role of gibberellins on leaf senescence may rely on the dosage or the situation of the treated leaves [46].
Shade-induced changes in auxin levels have been found in sunflowers and tomatoes, and the transcription of auxin-response genes is dramatically affected after being treated with shade conditions [21][47]. Low R:FR induced the expression of tryptophan aminotransferase of Arabidopsis 1 (TAA1), an aminotransferase that catalyzes the formation of indole-3-pyruvic acid from L-tryptophan in the auxin biosynthetic pathway, and TAA1-Related proteins (TAR) [48]. On the other hand, low R:FR also stimulates YUCCA gene expression through PIF TFs. Thus, shade conditions promote auxin accumulation in the shoot and the elongating hypocotyl [49]. Low R:FR upregulates the expression of GA20ox1 and GA20ox2, which are responsible for the production of bioactive GAs and promotes the accumulation of bioactive GAs [50]. Bioactive GAs interacts with GA receptor GID1, leading to ubiquitination and degradation of DELLA proteins [51]. The abundance of DELLA proteins does decrease in response to the increase in planting density and low R:FR ratio [52].
Confusingly, the increased level of growth-promoting phytohormone is not consistent with the accelerated leaf senescence phenotype under shade conditions. It is possible that shade-induced growth-promoting hormones such as auxin, gibberellin, and cytokinin function in the shoot or emerging apical meristem, promote stem elongation and help a shaded plant to outcompete its neighbors for light-absorbing, not in the mature leaves. However, the senescence-promoting phytohormones, such as ethylene and abscisic acid, function in the mature leaves to accelerate leaf senescence.

6. Growth-Defense Phytohormones Jamonic Acid and Salicylic Acid

Jasmonic acid (JA) and salicylic acid (SA) are crucial for plant defense against both biotic and abiotic stresses. The exogenous application of methyl jasmonate accelerates the process of leaf senescence by enhancing the transcriptional levels of senescence-associated genes such as SEN4 and SAG21 [53]. The transcript abundance of components is responsible for JA synthesis and signaling increases during the initial stage of leaf senescence [18]. Consistent with this, Arabidopsis leaves undergoing senescence exhibit 4-fold increase in JA content compared to nonsenescing leaves [54]. Disruption of 3-ketoacyl-CoA thiolase 2 (KAT2), the beta-oxidation gene involved in JA biosynthesis, delays dark-induced leaf senescence [55]. JA is thought to integrate stress signals to induce the onset of leaf senescence in an age-dependent manner, given that older leaves experience a more rapid senescence process than younger leaves after exogenous application with methyl jasmonate [42]. Shade treatment can suppress the natural defense mechanisms activated by JA signaling and the expression of genes related to defense [56]. This effect is partially due to the inactivation of phyB by shade, which attenuates JA sensitivity by stabilizing PIFs and JAZs (jasmonate ZIM domains) while destabilizing DELLA proteins. As a result, this facilitates the ability of PIFs and JAZs to activate downstream target genes without being inhibited by DELLA proteins [57][58][59]. Additionally, miR319 can promote leaf senescence by downregulating teosinte branched 1 cycloidea, PCF (TCP) transcription factors, which in turn boosts the level of JA [15].
SA, as a phytohormone known to promote senescence, both initiates and accelerates leaf senescence [60]. Mutant plants, such as the phytoalexin deficient 4 (pad 4) and nonexpresser of pathogen-related genes (npr1) mutants, exhibit delayed leaf senescence [61]. During senescence, many genes related to SA biosynthesis and signaling are upregulated, and treatment with SA markedly induces the expression of SAGs, including SEN1 and WRKY transcriptional factors WRKY6, WRKY53, WRKY54, and WRKY70 [42]. When grown under shade, the inactivation of phyB leads to a decrease in SA-mediated defense against pathogen attacks. Low R:FR ratios cause significant changes in the expression of SA-related genes. Plants with impaired SA biosynthesis or signaling are unable to elongate properly in response to Low R:FR ratios [62]. Interestingly, although the content of SA itself remains unchanged under low R:FR light, the degree of SA-dependent phosphorylation of nonexpressor of pathogenesis-related genes 1 (NPR1), a key transcriptional regulator of SA-mediated defense, is reduced [62]. This resource reallocation can attenuate the resistance to abiotic and biotic stresses under shade conditions, as defense mechanisms are hampered by the need for rapid stem elongation.

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Zhuang Li
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Tao Zhao
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Jun Liu
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Hongyu Li
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Bin Liu
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