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High concentrations of heavy metal (HM) ions impact agronomic staple crop production in acid soils (pH ≤ 5) due to their cytotoxic, genotoxic, and mutagenic effects. Among cytotoxic ions, the trivalent aluminum cation (Al3+) formed by solubilization of aluminum (Al) into acid soils, is one of the most abundant and toxic elements under acidic conditions. In recent years, several studies have elucidated the different signal transduction pathways involved in HM responses, identifying complementary genetic mechanisms conferring tolerance to plants. Although epigenetics has become more relevant in abiotic stress studies, epigenetic mechanisms underlying plant responses to HM stress remain poorly understood. This review describes the main epigenetic mechanisms related to crop responses during stress conditions, specifically, the molecular evidence showing how epigenetics is at the core of plant adaptation responses to HM ions. We highlight the epigenetic mechanisms that induce Al tolerance. Likewise, we analyze the pivotal relationship between epigenetic and genetic factors associated with HM tolerance. Finally, using rice as a study case, we performed a general analysis over previously whole-genome bisulfite-seq published data. Specific genes related to Al tolerance, measured in contrasting tolerant and susceptible rice varieties, exhibited differences in DNA methylation frequency. The differential methylation patterns could be associated with epigenetic regulation of rice responses to Al stress, highlighting the major role of epigenetics over specific abiotic stress responses.

Soil salinity is an abiotic stress that reduces agricultural productivity. For decades, halophytes have been studied to elucidate the physiological and biochemical processes involved in alleviating cellular ionic imbalance and conferring salt tolerance. Recently, several interesting genes with proven influence on salt tolerance were isolated from the Mediterranean halophyte Lobularia maritima (L.) Desv. A better understanding of salt response in this species is needed to exploit its potential as a source of stress-related genes. We report the characterisation of L. maritima’s response to increasing NaCl concentrations (100–400 mM) at the physiological, biochemical and molecular levels. L. maritima growth was unaffected by salinity up to 100 mM NaCl and it was able to survive at 400 mM NaCl without exhibiting visual symptoms of damage. Lobularia maritima showed a Na+ and K+ accumulation pattern typical of a salt-includer halophyte, with higher contents of Na+ in the leaves and K+ in the roots of salt-treated plants. The expression profiles of NHX1, SOS1, HKT1, KT1 and VHA-E1 in salt-treated plants matched this Na+ and K+ accumulation pattern, suggesting an important role for these transporters in the regulation of ion homeostasis in leaves and roots of L. maritima. A concomitant stimulation in phenolic biosynthesis and antioxidant enzyme activity was observed under moderate salinity, suggesting a potential link between the production of polyphenolic antioxidants and protection against salt stress in L. maritima. Our findings indicate that the halophyte L. maritima can rapidly develop physiological and antioxidant mechanisms to adapt to salt and manage oxidative stress.

Halophyte Lobularia maritima LmSAP encodes an A20AN1 zinc-finger stress-associated protein which expression is up-regulated by abiotic stresses and heavy metals in transgenic tobacco. To deepen our understanding of LmSAP function, we isolated a 1,147 bp genomic fragment upstream of LmSAP coding sequence designated as PrLmSAP. In silico analyses of PrLmSAP revealed the presence of consensus CAAT and TATA boxes and cis-regulatory elements required for abiotic stress, phytohormones, pathogen, and wound responses, and also for tissue-specific expression. The PrLmSAP sequence was fused to the β-glucuronidase (gusA) reporter gene and transferred to rice. Histochemical GUS staining showed a pattern of tissue-specific expression in transgenic rice, with staining observed in roots, coleoptiles, leaves, stems and floral organs but not in seeds or in the root elongation zone. Wounding strongly stimulated GUS accumulation in leaves and stems. Interestingly, we observed a high stimulation of the promoter activity when rice seedlings were exposed to NaCl, PEG, ABA, MeJA, GA, cold, and heavy metals (Al3+, Cd2+, Cu2+ and Zn2+). These results suggest that the LmSAP promoter can be a convenient tool for stress-inducible gene expression and is a potential candidate for crop genetic engineering.