The MAPK signaling pathway functions as a universally preserved mechanism in eukaryotic organisms for transmitting signals from the cell exterior (Huang et al., 2022). The MAPK cascade participates in plants’ response to manage abiotic stress (de Zelicourt et al., 2016). MAPKs are structurally highly conserved serine/threonine protein kinases; they phosphorylate diverse substrates, for example, cytoskeleton-related proteins, protein kinases, and transcription factors; moreover, they have key functions in controlling how plants respond to stress, such as drought, heavy metals, extreme temperatures, and salinity (Moustafa et al., 2014; Gao et al., 2019). MAPK, MAPKK, and MAPKKK are the three distinct sets of protein kinases in the MAPK cascade. These kinases activate one another sequentially through phosphorylation (Danquah et al., 2014). Typically, MAP3Ks are activated through extracellular signals. The activated MAP3Ks then induce phosphorylation and activation of the S/T-X_3-5-S/T motif present in downstream MAPKKs. Next, the activated MAPKKs stimulate the phosphorylation and activation of MAPKs at the TXY activation loop, thereby facilitating signal transmission to the nucleus ( Figure 1 ) (Tena et al., 2001; Meng and Zhang, 2013; Jiang et al., 2022). MAPKKKs, may serve as adaptors to establish a link between upstream signaling events and the main MAPK cascades.

The complete Arabidopsis thaliana genome sequence revealed 20 genes potentially encoding MAPKs. In tomato, 16 SlMAPKs have been identified. These MAPKs are divided into four groups ( Figure 2 ) (MAPK Group, 2002; Kong et al., 2012). SlMAPK1-3, SlMAPK4-7, SlMAPK8 and 9, and SlMAPK10-16 were included in Groups A, B, C, and D, respectively. Conserved domain analysis shows that members of the A, B, and C subfamilies have a Thr-Glu-Tyr (TEY) phosphorylation motif in their active sites, while members of the D subfamily have a Thr-Asp-Tyr (TDY) motif in their active sites (Kong et al., 2012). MAPKs of Group A, specifically Arabidopsis thaliana MAPK3 and MAPK6, were initially associated with plant defense mechanisms and responses to abiotic stresses. Subsequently, their significant contributions to plant development and growth were also demonstrated (Wang et al., 2023; Wu et al., 2024; Wu and Wang, 2024).

Group B MAPKs, such as Arabidopsis thaliana MAPK4, MAPK5, MAPK11, MAPK12, and MAPK13, play roles in plant immune responses, adaptation to environmental conditions, and plant development and growth (de Zelicourt et al., 2016; Thulasi Devendrakumar et al., 2018). Furthermore, Group C MAPKs, including Arabidopsis thaliana MAPK1, MAPK2, MAPK7, and MAPK14, along with MAP3K17/18, constitute the MAP3K17/18-MKK3-MAPK1/2/7/14 cascade; these MAPKs have important functions in abscisic acid (ABA) signaling, senescence, and tolerance to drought (Matsuoka et al., 2015; Li et al., 2017; Tajdel-Zielińska et al., 2024). Groups A-C included the TEY subtype MAPKs, while Group D MAPK is a TDY subtype with eight members in Arabidopsis thaliana: MAPK8, MAPK9, MAPK15, MAPK16, MAPK17, MAPK18, MAPK19, and MAPK20. Compared to the members of Group A-C, Group D members possess a longer C-terminal region and show absence of the common MAPKK-binding docking motif (Dóczi et al., 2012; Zhang and Zhang, 2022). MAPK9, a Group D member, is activated independent of upstream MAPKKs; it is activated by autophosphorylation. Furthermore, BRASSINOSTEROID-SIGNALING KINASE1 modulates the phosphorylation of MAPK15 to induce resistance in Arabidopsis thaliana to powdery mildew (Nagy et al., 2015; Shi et al., 2022). Thus, MAPKs are pivotal in enabling overall development and growth of plants and in interacting with biotic and abiotic stresses.

Drought, one of the major abiotic stress, severely impacts crop production. It not only has drastic effects on plant productivity and metabolism but also leads to widespread socioeconomic burden and damage (Lesk et al., 2016). Several biochemical and transcriptional studies have shown that MAPKs are involved in tomato plant’s response to drought. SlMAPK1 has a pivotal function in how plants respond to abiotic stressors such as drought. As reported previously, SlMAPK1 contributes to JA biosynthesis, a hormone essential for plant defense and stress response (Alfagham et al., 2024). During drought, SlMAPK1 activation increases JA levels, thereby improving the plant’s capacity to withstand dehydration and recuperate from water deficiency. JA is crucial for stomatal closure, which reduces transpiration-mediated loss of water, as well as for root growth that enhances water absorption from soil (Alfagham et al., 2024; Wang et al., 2018). Furthermore, SlMAPK1 interacts with various proteins and transcription factors within the MAPK pathway, thereby activating genes that facilitate plant acclimation to drought stress. Previous research has also indicated that the metabolite albaflavenone, produced by microbial endophytes, improves drought resistance in tomato plants by activating the SlMAPK1 protein in the MAPK signaling pathway (Alfagham et al., 2024). SlMAPK3 has a remarkable function in responding to abiotic stress events, for example, stress due to heavy metals (cadmium) and drought (Muhammad et al., 2019). SlMAPK3 gene knockdown by CRISPR/Cas9 gene editing technology increased tomato plants’ sensitivity to drought stress, led to greater membrane damage, and reduced antioxidant enzyme activity (Wang et al., 2017a). In contrast, transgenic plants overexpressing SlMAPK3 showed enhanced antioxidant enzyme activity and improved tolerance to stress due to drought and cadmium exposure. These findings revealed the function of SlMAPK3 in regulating antioxidant responses and protecting cellular membrane in tomato plants, thus suggesting potential molecular mechanisms for developing tomato varieties with elevated abiotic stress tolerance (Wang et al., 2017a; Muhammad et al., 2019; Huang et al., 2023). Compared to control plants, SlMAPK4 gene silencing diminished drought stress tolerance, resulting in earlier wilting in drought (Virk et al., 2013). Additionally, silencing of SlMAPK4 in tomato plants upregulated the expression of Pathogenesis-Related 1a (SlPR1a) and SlPR1b, which are defense-related genes. Thus, in tomato, SlMAPK4 may participate in salicylic acid (SA) - and JA/ET-mediated signaling pathways (Nambeesan et al., 2012; Virk et al., 2013).

Carbon monoxide (CO), nitric oxide (NO), and hydrogen sulfide (H₂S) are the three endogenously produced gaseous signaling molecules (Yamasaki and Cohen, 2016). Exogenous H₂S and NO treatment enhances plant stress tolerance against harsh environments, including extreme temperatures, salinity, and drought, by enhancing antioxidant systems and cellular resistance (Tian et al., 2016; Ni et al., 2016; Kolbert, 2019). The MAPK signaling pathway facilitates the promotion of tomato seedling growth by H₂S, and some MAPK family genes, particularly SlMAPK3 and SlMAPK13, exhibit remarkably altered expression pattern following exogenous addition of NaHS The MAPK inhibitor PD98059 reduces H₂S levels and L-cysteine demercase (LCD) activity in tomato seedlings (Ba et al., 2021). SNP, an NO donor, at 100 μM concentration effectively promotes tomato seedling growth, enhances nitrogen metabolism, and minimizes oxidative damage in low nitrogen stress condition. The molecular response to low nitrogen concentration stress and NO treatment in tomato seedlings involves the MAPK pathway as a key factor (Zhang et al., 2022b; Lu et al., 2024). PD98059, the MAPK inhibitor, weakens NO effects, thus suggesting that, in low nitrogen concentration stress condition, the MAPK signaling pathway mediates NO-based nitrogen metabolism and abolition of oxidative damage and growth inhibition in tomato seedlings (Ba et al., 2021; Zhang et al., 2022b; Lu et al., 2024).

Temperature significantly impacts plant productivity and growth. Plants can thrive within a specific temperature range; however, extreme temperatures can cause damage to plant cells. Cold stress inhibits germination, growth, and metabolism and disrupts membranes by forming ice crystals. High temperatures induce heat stress, increase respiration, and cause ROS overproduction, thereby impacting plant productivity and growth (Moustafa et al., 2014; Wu et al., 2022; Manasa et al., 2022; Kan et al., 2023). MAPKs are critically involved in temperature signal perception and transduction (Sangwan and Dhindsa, 2002). MAPKs and C-repeat binding factors (CBF) have essential functions in monitoring cold response. Exogenous hydrogen peroxide treatment improves tomato plants tolerance to cold stress by stimulating SlCBF1 and SlMAPK1/2/3 expression and modulating antioxidant enzyme activity and phytohormone levels (Wang et al., 2017b). SlMAPK3 knockout resulted in reduced content of ferulic acid (FA) and inhibition of FA synthesis-associated gene expression (SlC3H, SlC4H, SlCOMT, and SlPAL5) (Kumar and Pruthi, 2014; Song et al., 2023). Specifically, FA showed reduced effects on osmotic regulatory substances and antioxidant enzymes together with a decline in CBF pathway-associated gene expression. These results revealed that FA positively contributes to the resistance of tomato fruits to chilling stress through MAPK3-dependent upregulation of genes linked with the CBF transcriptional pathway (Miura et al., 2012; Shu et al., 2022). Remarkably, SlMAPK1 and SlMAPK2 are crucial for mediating B-box (SlBBX17) proteins phosphorylation. This phosphorylation event enhances the formation of a complex between SlHY5 and SlBBX17, which then modulates the activity of SlCBFs, ultimately conferring low-temperature tolerance to the plants (Heng et al., 2019; Song et al., 2023).

In tomato plants, the SlMAPK3 gene participates in environmental stress response, particularly to temperature stress (Yu et al., 2019). SlMAPK3 gene knockout enhances heat stress tolerance through the prevention of ROS accumulation as well as elevation of the expression levels of heat stress transcription factors (HSFs), antioxidant enzymes, and heat shock proteins (Iba, 2002; Yu et al., 2019). Conversely, SlMAPK3 overexpression in tobacco enhances low-temperature-stress tolerance by activating cellular antioxidant systems, altering stress-responsive gene transcription, and improving ROS scavenging- and stress tolerance-associated gene expression. Collectively, these findings highlight the critical regulatory function of SlMAPK3 in plants’ response to temperature stress (Yu et al., 2015a, 2019). SlMAPK7 is a Group B MAPK gene. As shown previously, SlMAPK7 responds to various stresses and signaling molecules, and its mRNA expression level is regulated by H₂O₂ and calcium ions (Ca²⁺). SlMAPK7 is localized primarily in the cell nucleus, and its overexpression enhances cold stress tolerance in transgenic tomato plants (Yu et al., 2015b). This enhancement is linked to cellular antioxidant system activation, modulation of stress-related gene expression, and more efficient scavenging of ROS. Thus, SlMAPK7 positively regulates plant cell response to cold stress by altering ROS homeostasis and affecting stress-responsive gene expression (Xing et al., 2008; Pitzschke et al., 2009; Yu et al., 2015b). Thus, MAPK signaling is a critical input for plants to recognize and act to tolerate temperature stress and to regulate cold tolerance by activating key pathways and transcription factors, which ultimately enhance growth and productivity under extreme conditions.

The occurrence of extreme weather events has increased recently, with high temperature (HT) being a notable example. Such elevated temperatures have become a primary environmental condition affecting the overall development and growth of crops (Teshome et al., 2020). In tomato plants, heat stress activates MAPKs. Heat-activated MAPK phosphorylates and promotes HSF clade A3 (HsfA3) expression (Link et al., 2002). The increased focus on MAPK-mediated responses to HT is noteworthy. SlMAPK1 silencing improves the heat tolerance of tomato plants, whereas SlMAPK1 overexpression leads to a decrease in heat tolerance in transgenic tomatoes. Additionally, following exposure to heat stress, the levels of antioxidant defense proteins in plants with SlMAPK1 interference are markedly increased, while plants with SlMAPK1 overexpression show a reduction in antioxidant defense capacity (Ding et al., 2018). SlMAPK1 interacts with the serine-proline-rich protein homology (SlSPRH1) and phosphorylates its Ser-44 site. This interaction regulates the antioxidant defense protein, which participates in response to HT, thus negatively regulating tomatoes’ tolerance to HT (Ding et al., 2018; Mo et al., 2021). CRISPR/Cas9-mediated slmapk3 mutants exhibited more tolerance to heat stress than WT plants, suggesting that SlMAPK3 was a negative regulator of thermotolerance (Yu et al., 2019). Additionally, the expression of antioxidant enzymes and heat shock proteins/heat shock factors (HSPs/HSFs) genes played a role in the heat stress response mediated by SlMAPK3 in tomato plants (Yu et al., 2019; Mo et al., 2021). SlMAPK11 is a novel gene that influences tomato seed germination, with higher expression in seeds adapted to lower germination temperatures (Song et al., 2021). Overexpression of SlMAPK11 reduces tomato seed germination and increases ABA sensitivity by upregulating 9-cis-epoxycarotenoid dioxygenase (NCED1) and affecting ABA signaling through SNF1-related kinase 2.2 (SnRK2.2) phosphorylation (Lefebvre et al., 2006; Song et al., 2021). Additionally, MAPK11 interacts with SnRK1, potentially inhibiting its activation and influencing ABA-insensitive 5 (ABI5) transcription (Song et al., 2021). Thus, MAPKs have relevant functions in tomato plants in responding to drought and temperature stress, mainly by regulating signaling pathways and antioxidant systems to enhance tomato tolerance.