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Phytosulfokine (PSK) is a disulfated pentapeptide that is an important signaling molecule. Although it has recently been implicated in plant defenses to pathogen infection, the mechanisms involved remain poorly understood. Using surface plasmon resonance and gene silencing approaches, we showed that the tomato (Solanum lycopersicum) PSK receptor PSKR1, rather than PSKR2, functioned as the major PSK receptor in immune responses. Silencing of PSK signaling genes rendered tomato more susceptible to infection by the economically important necrotrophic pathogen Botrytis cinerea. Analysis of tomato mutants defective in either defense hormone biosynthesis or signaling demonstrated that PSK-induced immunity required auxin biosynthesis and associated defense pathways. Here, using aequorin-expressing tomato plants, we provide evidence that PSK perception by tomato PSKR1 elevated cytosolic [Ca2+], leading to auxin-dependent immune responses via enhanced binding activity between calmodulins and the auxin biosynthetic YUCs. Thus, our data demonstrate that PSK acts as a damage-associated molecular pattern and is perceived mainly by PSKR1, which increases cytosolic [Ca2+] and activates auxin-mediated pathways that enhance immunity of tomato plants to B. cinerea.

Summary The ability to interpret daily and seasonal fluctuations, latitudinal and vegetation canopy variations in light and temperature signals is essential for plant survival. However, the precise molecular mechanisms transducing the signals from light and temperature perception to maintain plant growth and adaptation remain elusive. We show that far‐red light induces PHYTOCHROME‐INTERACTING TRANSCRIPTION 4 (SlPIF4) accumulation under low‐temperature conditions via phytochrome A in Solanum lycopersicum (tomato). Reverse genetic approaches revealed that knocking out SlPIF4 increases cold susceptibility, while overexpressing SlPIF4 enhances cold tolerance in tomato plants. SlPIF4 not only directly binds to the promoters of the C‐REPEAT BINDING FACTOR (SlCBF) genes and activates their expression but also regulates plant hormone biosynthesis and signals, including abscisic acid, jasmonate and gibberellin (GA), in response to low temperature. Moreover, SlPIF4 directly activates the SlDELLA gene (GA‐INSENSITIVE 4, SlGAI4) under cold stress, and SlGAI4 positively regulates cold tolerance. Additionally, SlGAI4 represses accumulation of the SlPIF4 protein, thus forming multiple coherent feed‐forward loops. Our results reveal that plants integrate light and temperature signals to better adapt to cold stress through shared hormone pathways and transcriptional regulators, which may provide a comprehensive understanding of plant growth and survival in a changing environment.

Light signaling and phytohormones both influence plant growth, development, and stress responses; however, cross talk between these two signaling pathways in response to cold remains underexplored. Here, we report that far-red light (FR) and red light (R) perceived by phytochrome A (phyA) and phyB positively and negatively regulated cold tolerance, respectively, in tomato (Solanum lycopersicum), which were associated with the regulation of levels of phytohormones such as abscisic acid (ABA) and jasmonic acid (JA) and transcript levels of ABA- and JA-related genes and the C-REPEAT BINDING FACTOR (CBF) stress signaling pathway genes. A reduction in the R/FR ratio did not alter cold tolerance, ABA and JA accumulation, and transcript levels of ABA- and JA-related genes and the CBF pathway genes in phyA mutant plants; however, those were significantly increased in wild-type and phyB plants with the reduction in the R/FR ratio. Even though low R/FR treatments did not confer cold tolerance in ABA-deficient (notabilis [not]) and JA-deficient (prosystemin-mediated responses2 [spr2]) mutants, it up-regulated ABA accumulation and signaling in the spr2 mutant, with no effect on JA levels and signaling in the not mutant. Foliar application of ABA and JA further confirmed that JA functioned downstream of ABA to activate the CBF pathway in light quality-mediated cold tolerance. It is concluded that phyA and phyB function antagonistically to regulate cold tolerance that essentially involves FR light-induced activation of phyA to induce ABA signaling and, subsequently, JA signaling, leading to an activation of the CBF pathway and a cold response in tomato plants.

Natural evolution has resulted in reduced cold tolerance in cultivated tomato ( Solanum lycopersicum ). Herein, we perform a combined analysis of ATAC-Seq and RNA-Seq in cold-sensitive cultivated tomato and cold-tolerant wild tomato ( S. habrochaites ). We identify that WRKY34 has the most significant association with differential chromatin accessibility and expression patterns under cold stress. We find that a 60 bp InDel in the WRKY34 promoter causes differences in its transcription and cold tolerance among 376 tomato accessions. This 60 bp fragment contains a GATA cis -regulatory element that binds to SWIBs and GATA29, which synergistically suppress WRKY34 expression under cold stress. Moreover, WRKY34 interferes with the CBF cold response pathway through regulating transcription and protein levels. Our findings emphasize the importance of polymorphisms in cis -regulatory regions and their effects on chromatin structure and gene expression during crop evolution. Cold tolerance has lost during tomato natural evolution. Here, the authors report that absence of a 60 bp promoter fragment in the WRKY34 gene results in loss of cold tolerance in domesticated tomato varieties, and reveal how this natural variation can affect cold tolerance.

• Light quality affects mutualisms between plant roots and arbuscular mycorrhizal fungi (AMFs), which modify nutrient acquisition in plants. However, the mechanisms by which light systemically modulates root colonization by AMFs and phosphate uptake in roots remain unclear. • We used a range of approaches, including grafting techniques, protein immunoblot analysis, electrophoretic mobility shift assay, chromatin immunoprecipitation, and dual-luciferase assays, to unveil the molecular basis of light signal transmission from shoot to root that mediates arbuscule development and phosphate uptake in tomato. • The results show that shoot phytochrome B (phyB) triggers shoot-derived mobile ELONGATED HYPOCOTYL5 (HY5) protein accumulation in roots, and HY5 further positively regulates transcription of strigolactone (SL) synthetic genes, thus forming a shoot phyB-dependent systemic signaling pathway that regulates the synthesis and accumulation of SLs in roots. Further experiments with carotenoid cleavage dioxygenase 7 mutants and supplementary red light confirm that SLs are indispensable in the red-light-regulated mycorrhizal symbiosis in roots. • Our results reveal a phyB–HY5–SLs systemic signaling cascade that facilitates mycorrhizal symbiosis and phosphate utilization in plants. The findings provide new prospects for the potential application of AMFs and light manipulation to effectively improve nutrient utilization and minimize the use of chemical fertilizers and associated pollution.

Calvin cycle is a sequence of enzymatic reactions that assimilate atmospheric CO 2 in photosynthesis. Multiple components are known to participate in the induction or suppression of the Calvin cycle but the mechanism of its regulation by phytohormones is still unclear. Brassinosteroids (BRs) are steroid phytohormones that promote photosynthesis and crop yields. In this study, we study the role of BRs in regulating Calvin cycle genes to further understand the regulation of the Calvin cycle by phytohormones in tomatoes. BRs and their signal effector BRASSINAZOLE RESISTANT 1 (BZR1) can enhance the Calvin cycle activity and improve the photosynthetic ability. BRs increased the accumulation of dephosphorylated form of BZR1 by 94% and induced an 88–126% increase in the transcription of key genes in Calvin cycle FBA1, RCA1, FBP5 , and PGK1 . BZR1 activated the transcription of these Calvin cycle genes by directly binding to their promoters. Moreover, silencing these Calvin cycle genes impaired 24-epibrassinolide (EBR)-induced enhancement of photosynthetic rate, the quantum efficiency of PSII, and V c,max and J max . Taken together, these results strongly suggest that BRs regulate the Calvin cycle in a BZR1-dependent manner in tomatoes. BRs that mediate coordinated regulation of photosynthetic genes are potential targets for increasing crop yields.

Strigolactones are carotenoid-derived phytohormones that impact plant growth and development in diverse ways. However, the roles of strigolactones in the responses to temperature stresses are largely unknown. Here, we demonstrated that strigolactone biosynthesis is induced in tomato (Solanum lycopersicum) by heat and cold stresses. Compromised strigolactone biosynthesis or signaling negatively affected heat and cold tolerance, while application of the synthetic strigolactone analog GR245DS enhanced heat and cold tolerance. Strigolactone-mediated heat and cold tolerance was associated with the induction of abscisic acid (ABA), heat shock protein 70 (HSP70) accumulation, C-REPEAT BINDING FACTOR 1 (CBF1) transcription, and antioxidant enzyme activity. Importantly, a deficiency in ABA biosynthesis compromised the GR245DS effects on heat and cold stresses and abolished the GR245DS-induced transcription of HSP70, CBF1, and antioxidant-related genes. These results support that strigolactones positively regulate tomato heat and cold tolerance and that they do so at least partially by the induction of CBFs and HSPs and the antioxidant response in an ABA-dependent manner.

Plant responses to elevated CO₂ and heat stress are tightly regulated by an intricate network of phytohormones. Plants accumulate ethylene (ET), the smallest hormone, in response to heat stress; however, the role of ET and its signaling in elevated CO₂-induced heat stress response remains largely unknown. In this study, we found that transcript levels of multiple genes relating to ET synthesis, signaling, and heat shock proteins (HSPs) were induced by elevated CO₂ (800 µmol mol⁻¹) compared to ambient CO₂ (400 µmol mol⁻¹) in tomato leaves under controlled temperature conditions (25°C). Elevated CO₂-induced responses to heat stress (42°C) were closely associated with increased ET production and HSP70 expression at both transcript and protein levels. Pretreatment with an antagonist of ET, 1-methylcyclopropene that inhibits ET-dependent responses, abolished elevated CO₂-induced stress response without affecting the ET production rate. In addition, silencing of ethylene response factor 1 (ERF1) compromised elevated CO₂-induced responses to heat stress, which was associated with the concomitant reduction in the transcript of heat shock factor A2, HSP70 and HSP90, indicating that ERF1 is required for elevated CO₂-induced responses to heat. All these results provide convincing evidence on the importance of ET biosynthesis and signaling in elevated CO₂-induced heat stress response in tomato plants. Thus, the study advances our understanding of the mechanisms of elevated CO₂-induced stress response and may potentially be useful for breeding heat-tolerant tomatoes in the era of climate change.

Autophagy, as an intracellular degradation system, plays a critical role in plant immunity. However, the involvement of autophagy in the plant immune system and its function in plant nematode resistance are largely unknown. Here, we show that root-knot nematode (RKN; Meloidogyne incognita ) infection induces autophagy in tomato ( Solanum lycopersicum ) and different atg mutants exhibit high sensitivity to RKNs. The jasmonate (JA) signaling negative regulators JASMONATE-ASSOCIATED MYC2-LIKE 1 (JAM1), JAM2 and JAM3 interact with ATG8s via an ATG8-interacting motif (AIM), and JAM1 is degraded by autophagy during RKN infection. JAM1 impairs the formation of a transcriptional activation complex between ETHYLENE RESPONSE FACTOR 1 (ERF1) and MEDIATOR 25 (MED25) and interferes with transcriptional regulation of JA-mediated defense-related genes by ERF1. Furthermore, ERF1 acts in a positive feedback loop and regulates autophagy activity by transcriptionally activating ATG expression in response to RKN infection. Therefore, autophagy promotes JA-mediated defense against RKNs via forming a positive feedback circuit in the degradation of JAMs and transcriptional activation by ERF1. Autophagy plays a critical role in plant immunity. Here the authors show that in tomato, autophagy promotes defense against root-knot nematodes by promoting degradation of negative regulators of jasmonic acid signaling.

Heavy metal pollution often occurs together with organic contaminants. Brassinosteroids (BRs) induce plant tolerance to several abiotic stresses, including phenanthrene (PHE) and cadmium (Cd) stress. However, the role of BRs in PHE+Cd co-contamination-induced stress amelioration is unknown. Here, the interactive effects of PHE, Cd, and 24-epibrassinolide (EBR; a biologically active BR) were investigated in tomato plants. The application of Cd (100 μM) alone was more phytotoxic than PHE applied alone (100 μM); however, their combined application resulted in slightly improved photosynthetic activity and pigment content compared with Cd alone after a 40 d exposure. Accumulation of reactive oxygen species and membrane lipid peroxidation were induced by PHE and/or Cd; however, the differences in effect were insignificant between Cd and PHE+Cd. The foliar application of EBR (0.1 μM) to PHE- and/or Cd-stressed plants alleviated photosynthetic inhibition and oxidative stress by causing enhancement of the activity of the enzymes and related transcript levels of the antioxidant system, secondary metabolism, and the xenobiotic detoxification system. Additionally, PHE and/or Cd residues were significantly decreased in both the leaves and roots after application of EBR, more specifically in PHE+Cd-stressed plants when treated with EBR, indicating a possible improvement in detoxification of these pollutants. The findings thus suggest a potential interaction of EBR and PHE for Cd stress alleviation. These results advocate a positive role for EBR in reducing pollutant residues for food safety and also strengthening phytoremediation.