Editorial: [Integrated Molecular Mechanisms of Plant Stress Responses: Insights from Transcriptomics, Metabolomics, and Gene Family Evolution]

Xiaobo Luo¹Georgia Ntatsi^2*Rong Zhou^3*Mintao Sun^4*

• ¹Guizhou Institute of Biotechnology, Guizhou Academy of Agricultural Sciences, Guiyang, Guizhou Province, China
• ²Laboratory of Vegetable Production, Department of Crop Science, Agricultural University of Athens, Athens, Greece
• ³Sanya Institute of Nanjing Agricultural University, Nanjing Agricultural University, Sanya, China
• ⁴Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, China

Plants face a multitude of biotic and abiotic stresses that threaten their growth, development, and productivity. Biotic stresses, such as fungal infections, and abiotic stresses, including drought, salinity, and temperature extremes, activate complex molecular networks involving transcriptional reprogramming, metabolic adjustments, and signaling cascades. Recent advancements in omics technologies have enabled comprehensive exploration of these mechanisms across diverse plant species. This review synthesizes findings from six studies on lily (Lilium spp.), licorice (Glycyrrhiza uralensis), potato (Solanum tuberosum), rice (Oryza sativa), soybean (Glycine max), and pigeonpea (Cajanus cajan), focusing on their molecular strategies to combat stress. By integrating transcriptomic, metabolomic, and gene family analyses, we highlight conserved pathways, species-specific adaptations, and future directions for crop improvement.In this research topic Chang et al., 2024 showed that Fusarium oxysporum-induced lily bulb rot triggers dynamic transcriptomic shifts, with 3,922, 7,595, and 6,590 DEGs at early (LYBH2), mid-(LYBH3), and late-stage (LYBH4) infection, respectively. In this study, key upregulated TFs-WRKY (regulating lignin via SA/JA signaling; Rushton et al., 1996;Deng et al., 2023) and AP2/ERF (modulating SA/ET/JA pathways; Ma et al., 2017) were found to drive phenylpropanoid-derived antimicrobials.The metabolomic analysis identified stage-specific flavonoids: Kaempferol-3-Orutinoside-7-O-rhamnoside (LYBH2, antibacterial; Ma et al., 2017), quercetin-3-Oglucoside (LYBH3, antiviral;Wei et al., 2021), and lignification enhancers (LYBH4; Ninfali et al., 2020). Despite upregulated lignin genes (PAL, CCoAOMT; Sun et al., 2024), minimal metabolite shifts suggest post-transcriptional regulation.In the study of Wand et al., drought stress was found to reduce photosynthesis and water use efficiency (WUE), with non-stomatal limitations dominating under severe drought (SD). Rehydration restored WUE in moderate drought (MD) but not severe drought (SD), indicating irreversible damage (Qi et al., 2021). Moreover, the chlorophyll fluorescence parameters (Fv/Fm, ΦPSII) mirrored photosynthetic recovery under drought stress.The transcriptome analysis in this study, revealed that drought stress induced the expression of the PAO1, 4, 5 and P5CS genes to promote the accumulation of spermidine and proline, enhancing soybean drought tolerance. Moreover, the metabolome analysis also identified proline, DL-tryptophan, and phenylalanine as key osmolytes under drought stress. Proline accumulation in MD plants aligned with barley and wheat studies (Chmielewska et al., 2016), while tryptophan derivatives may correlate with antioxidant responses (Rabara et al., 2017). Integrated transcript-metabolite networks highlighted phenylpropanoid and amino acid pathways as critical hubs.Gao et al., revealed that the MAPK cascade, conserved across eukaryotes, transduces stress signals via phosphorylation (Jagodzik et al. 2018). In G. uralensis, 21GuMAPKs were classified into four subgroups (A-D) based on TEY/TDY activation motifs (López-Bucio et al., 2014). Subgroups A (GuMAPK3/6) and D (GuMAPK16) exhibited colinearity with Arabidopsis and tomato homologs, underscoring evolutionary conservation.Within GuMAPKs, gene duplication, particularly segmental duplication, drove functional diversification, as seen in three homologous pairs (Wang et al., 2021).Under 200 mM NaCl, GuMAPK5, 7, 9, and 16 were upregulated, while Bacillus subtilis inoculation further enhanced their expression, indicating microbial priming of salt tolerance. Protein interaction networks linked GuMAPKs to PR1 (pathogenesis-related protein) and RBOHD (ROS-generating NADPH oxidase), bridging biotic and abiotic stress responses (Yamada et al., 2016). At 300 mM NaCl, GuMAPK16-2 downregulation postinoculation suggested stress threshold modulation.Yin et al., discovered that potato tuberization is regulated by photoperiod-sensitive StCOL genes (Abelenda et al., 2016). Phylogenetic analysis classified StCOLs into three subfamilies with conserved motifs/structures (2-4 exons) and 10 motifs/6 PTMs affecting protein function. Synteny revealed 13 StCOLs share a common ancestor, highlighting evolutionary conservation.Cold-responsive StCOL2, 3, 9, and 15 contained lowtemperature cis-elements. StCOL9 downregulation post-chilling suggests its role as a negative regulator, akin to AtCOL1 in Arabidopsis (Mikkelsen & Thomashow, 2009). These genes likely integrate photoperiod and temperature cues to optimize tuberization under stress.Liu et al., explained that the ALOG domain, derived from retroposon recombinases, governs rice reproductive development (Turchetto et al., 2023). Phylogenetic analysis divided 14 OsG1L genes into six clades, with OsG1L1/2/5/6 regulating panicle architecture (Beretta et al., 2023). Collinearity between OsG1L3/4/5 and OsG1L7/8 suggested subfunctionalization. Rice ALOG promoters are enriched with ABA-responsive ABRE motifs (half with ≥5 ABREs; up to 12 in one member) and drought-linked MBS elements.Most ALOG genes are downregulated under ABA/drought, consistent with ABA-insensitive root/seed phenotypes in LSH8 mutants (promoter ABREs, nuclear localization; Zou et al., 2021). Similarly, OsG1L7 (9 ABREs, nuclear) is suppressed by ABA/drought, suggesting shared roles in ABA signaling. These findings highlight ALOG family involvement in ABAmediated stress responses via promoter cis-elements and transcriptional regulation.The study by Alekhya et al. conducted a comprehensive genomic and functional characterization of the BAG gene family in pigeonpea (Cajanus cajan), revealing critical insights into their role in heat stress response. Alekhya et al., demonstrated that Pigeonpea's nine BAGs genes (five chromosomes) show lineage-specific evolution via Whole Genome Duplication (WGD). UBL domains in BAG1/2/4 suggest ubiquitin roles, while BAG6's IQ motif links to calcium signaling. Phylogenetically, five clades (shared with tomato/soybean) reflect exon/intron divergence, with non-conserved structures (as in Arabidopsis, rice, wheat (Doukhanina et al., 2006;Rana et al., 2012;Ge et al., 2016) driving functional diversification.In heat-tolerant genotype TS3R, CcBAG4 (interacting with HSP70) was upregulated, suppressing cell death (Doukhanina et al., 2006).Conversely, CcBAG5/6 showed upregulation in susceptible lines, mirroring tomato SlBAG9 (homolog of AtBAG5) overexpression-induced heat sensitivity (Ding et al., 2022). miRNA targeting of CcBAG6 in TS3R suggested post-transcriptional silencing, enhancing thermotolerance.