Transcriptomics, proteomics, and metabolomics interventions prompt crop improvement against metal(loid) toxicity.

The escalating challenges posed by metal(loid) toxicity in agricultural ecosystems, exacerbated by rapid climate change and anthropogenic pressures, demand urgent attention. Soil contamination is a critical issue because it significantly impacts crop productivity. The widespread threat of metal(loid) toxicity can jeopardize global food security due to contaminated food supplies and pose environmental risks, contributing to soil and water pollution and thus impacting the whole ecosystem. In this context, plants have evolved complex mechanisms to combat metal(loid) stress. Amid the array of innovative approaches, omics, notably transcriptomics, proteomics, and metabolomics, have emerged as transformative tools, shedding light on the genes, proteins, and key metabolites involved in metal(loid) stress responses and tolerance mechanisms. These identified candidates hold promise for developing high-yielding crops with desirable agronomic traits. Computational biology tools like bioinformatics, biological databases, and analytical pipelines support these omics approaches by harnessing diverse information and facilitating the mapping of genotype-to-phenotype relationships under stress conditions. This review explores: (1) the multifaceted strategies that plants use to adapt to metal(loid) toxicity in their environment; (2) the latest findings in metal(loid)-mediated transcriptomics, proteomics, and metabolomics studies across various plant species; (3) the integration of omics data with artificial intelligence and high-throughput phenotyping; (4) the latest bioinformatics databases, tools and pipelines for single and/or multi-omics data integration; (5) the latest insights into stress adaptations and tolerance mechanisms for future outlooks; and (6) the capacity of omics advances for creating sustainable and resilient crop plants that can thrive in metal(loid)-contaminated environments.

The exogenous application of naringenin and rosmarinic acid modulates functional traits in Lepidium sativum.

BACKGROUND: Phenolic modulators have attracted attention for their potential in shaping functional traits in plants. This work investigated the impact of naringenin (Nar) and rosmarinic acid (RA) on the functional properties of Lepidium sativum leaves and roots. RESULTS: Untargeted metabolomics identified a diverse phenolic profile, including flavonoids, phenolic acids, low molecular weight phenolics, lignans, and stilbenes. Cluster, analysis of variance multiblock orthogonal partial least squares (AMOPLS), and orthogonal projection to latent structures discriminant analysis (OPLS-DA) multivariate analyses confirmed tissue-specific modulation of bioactive compounds. The tissue was the hierarchically most influential factor, explaining 27% of observed variability, while the treatment and their interaction were statistically insignificant. Thereafter, various in vitro assays were employed to assess antioxidant capacity, including 1,1-diphenyl-2-picrylhydrazyl (DPPH), 2,2'-azino-bis(3-ethylbenzothiazoline)-6-sulfonic acid (ABTS) radical scavenging activity, cupric ion reducing antioxidant capacity (CUPRAC), and ferric ion reducing antioxidant power (FRAP), metal chelating ability, and phosphomolybdenum (PMD) assays. Extracts were also tested for inhibitory effects on cholinesterase, amylase, glucosidase, and tyrosinase enzymes. RA application positively impacted antioxidant and enzyme inhibitory activities, holding valuable implications in shaping the health-promoting properties of L. sativum. CONCLUSION: The untargeted metabolomics analysis showed a significant tissue-dependent modulation of bioactive compounds, determining no synergistic effect between applying phenolic compounds in combination. Specifically, the sole application of RA increased anthocyanins and hydroxyphenyl propanoic acid content on leaves, which was strictly related to enhancing the biological activities. © 2023 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Foliar applications of a Malvaceae-derived protein hydrolysate and its fractions differentially modulate yield and functional traits of tomato under optimal and suboptimal nitrogen application.

BACKGROUND: Protein hydrolysates (PHs) can enhance plant nitrogen nutrition and improve the quality of vegetables, depending on their bioactive compounds. A tomato greenhouse experiment was conducted under both optimal (14 mM) and suboptimal (2 mM) nitrogen (N-NO3) conditions. Tomatoes were treated with a new Malvaceae-derived PH (MDPH) and its molecular fractions (MDPH1, >10 kDa; MDPH2, 1-10 kDa and MDPH3, <1 kDa). RESULTS: Under optimal N conditions, the plants increased biomass and fruit yield, and showed a higher photosynthetic pigment content in leaves in comparison with suboptimal N, whereas under N-limiting conditions, an increase in dry matter, soluble solid content (SSC) and lycopene, a reduction in firmness, and changes in organic acid and phenolic compounds were observed. With 14 mM N-NO3, MDPH3 stimulated an increase in dry weight and increased yield components and lycopene in the fruit. The MDPH2 fraction also resulted in increased lycopene accumulation in fruit under 14 mM N-NO3. At a low N level, the PH fractions showed distinct effects compared with the whole MDPH and the control, with an increase in biomass for MDPH1 and MDPH2 and a higher pigment content for MDPH3. Regardless of N availability, all the fractions affected fruit quality by increasing SSC, whereas MDPH2 and MDPH3 modified organic acid content and showed a higher concentration of flavonols, lignans, and stilbenes. CONCLUSION: The molecular weight of the peptides modifies the effect of PHs on plant performance, with different behavior depending on the level of N fertilization, confirming the effectiveness of fractioning processes. © 2024 Society of Chemical Industry.

The inclusion of engineered ZnO nanoparticles and bulk ZnSO4 in the growth medium distinctively modulate the root and leaf metabolome in bean plants.

Together with toxicity, beneficial effects on plant growth have been ascribed to nanoparticles (NPs). This study aimed to survey the growth performance and metabolome adjustment of beans grown in a growth medium containing ZnONPs at different concentrations and compared with bulk ZnSO4 as a positive control. Growth parameters showed a reduction in shoot height starting from the lowest (25 mg L-1 ) concentration of ZnONPs. In comparison, growth was inhibited from 50 mg L-1 ZnSO4 , suggesting more toxic effects of nano forms of Zn. Untargeted metabolomics allowed us to unravel the biochemical processes involved in both promising and detrimental aspects. Multivariate statistics indicated that the tested Zn species substantially and distinctively altered the metabolic profile of both roots and leaves, with more metabolites altered in the former (435) compared with leaves (381). Despite having Zn forms in the growth medium, also leaf metabolome underwent a significant and extensive modulation. In general, the elicitation of secondary metabolism (N-containing compounds, phenylpropanoids, and phytoalexins) and the down-accumulation of fatty acid biosynthesis compounds were common responses to different Zn forms. However, an opposite trend could be observed for amino acids, fatty acids, carbohydrates, and cofactors being down-accumulated in ZnONPs treatment. Osmolytes, especially in ZnSO4 treatment, contributed to mitigating the effect of Zn toxicity and maintaining plant growth. Overall, the results indicated a complexity of tissue-specific and Zn-dependent response differences, resulting in distinctive metabolic perturbations.

The comparative effects of manganese nanoparticles and their counterparts (bulk and ionic) in Artemisia annua plants via seed priming and foliar application.

The world has experienced an unprecedented boom in nanotechnology. Nanoparticles (NPs) are likely to act as biostimulants in various plants due to having high surface/volume value. However, understanding the actual effect of NPs is essential to discriminate them from other counterparts in terms of being applicable, safe and cost-effective. This study aimed to assay the impact of manganese(III) oxide (Mn2O3)-NPs via seed-priming (SP) and a combination of SP and foliar application (SP+F) on Artemisia. annua performance at several times intervals and comparison with other available manganese (Mn) forms. Our findings indicate that SP with MnSO4 and Mn2O3-NPs stimulates the processes that occur prior to germination and thus reduces the time for radicle emergence. In both applications (i.e., SP and +F), none of the Mn treatments did show adverse phytotoxic on A. annua growth at morpho-physio and biochemical levels except for Mn2O3, which delayed germination and further plant growth, subsequently. Besides, from physio-biochemical data, it can be inferred that the general mechanism mode of action of Mn is mainly attributed to induce the photosynthetic processes, stimulate the superoxide dismutase (SOD) activity, and up-regulation of proline and phenolic compounds. Therefore, our results showed that both enzymatic and non-enzymatic antioxidants could be influenced by the application of Mn treatments in a type-dependent manner. In general, this study revealed that Mn2O3-NPs at the tested condition could be used as biostimulants to improve germination, seedling development and further plant growth. However, they are not as effective as MnSO4 treatments. Nonetheless, these findings can be used to consider and develop Mn2O3-NPs priming in future studies to improve seed germination and seedling quality in plants.

Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants.

Due to global climate change, abiotic stresses are affecting plant growth, productivity, and the quality of cultivated crops. Stressful conditions disrupt physiological activities and suppress defensive mechanisms, resulting in stress-sensitive plants. Consequently, plants implement various endogenous strategies, including plant hormone biosynthesis (e.g., abscisic acid, jasmonic acid, salicylic acid, brassinosteroids, indole-3-acetic acid, cytokinins, ethylene, gibberellic acid, and strigolactones) to withstand stress conditions. Combined or single abiotic stress disrupts the normal transportation of solutes, causes electron leakage, and triggers reactive oxygen species (ROS) production, creating oxidative stress in plants. Several enzymatic and non-enzymatic defense systems marshal a plant's antioxidant defenses. While stress responses and the protective role of the antioxidant defense system have been well-documented in recent investigations, the interrelationships among plant hormones, plant neurotransmitters (NTs, such as serotonin, melatonin, dopamine, acetylcholine, and γ-aminobutyric acid), and antioxidant defenses are not well explained. Thus, this review discusses recent advances in plant hormones, transgenic and metabolic developments, and the potential interaction of plant hormones with NTs in plant stress response and tolerance mechanisms. Furthermore, we discuss current challenges and future directions (transgenic breeding and genome editing) for metabolic improvement in plants using modern molecular tools. The interaction of plant hormones and NTs involved in regulating antioxidant defense systems, molecular hormone networks, and abiotic-induced oxidative stress tolerance in plants are also discussed.

Foliar Application of CeO2 Nanoparticles Alters Generative Components Fitness and Seed Productivity in Bean Crop (Phaseolus vulgaris L.).

In the era of technology, nanotechnology has been introduced as a new window for agriculture. However, no attention has been paid to the effect of cerium dioxide nanoparticles (nCeO2) on the reproductive stage of plant development to evaluate their toxicity and safety. To address this important topic, bean plants (Phaseolus vulgaris L.) treated aerially with nCeO2 suspension at 250-2000 mg L-1 were cultivated until flowering and seed production in the greenhouse condition. Microscopy analysis was carried out on sectioned anthers and ovules at different developmental stages. The pollen's mother cell development in nCeO2 treatments was normal at early stages, the same as control plants. However, the results indicated that pollen grains underwent serious structural damages, including chromosome separation abnormality at anaphase I, pollen wall defect, and pollen grain malformations in nCeO2-treated plants at the highest concentration, which resulted in pollen abortion and yield losses. On the ovule side, the progression of development only at the highest concentration was modified in the two-nucleated embryo sac stage, probably due to apoptosis in nuclei. Nevertheless, the findings confirmed the more pronounced vulnerability of male reproductive development under nCeO2 exposure than female development. The higher concentration decreased seed productivity, including seed set in either pods or whole plant (13% and 18% compared to control, respectively). The data suggested the potential application of nCeO2 at optimal dosages as a plant productivity ameliorative. However, a higher dosage is considered as an eco-environmental hazard. To our best knowledge, this is the first study analyzing reproductive plant response upon exposure to nCeO2.

Aerially Applied Zinc Oxide Nanoparticle Affects Reproductive Components and Seed Quality in Fully Grown Bean Plants (Phaseolus vulgaris L.).

The development of reproductive components in plant species is susceptible to environmental stresses. The extensive application of zinc oxide nanoparticles (nZnO) in various agro-industrial processes has jeopardized the performance and functionality of plants. To understand the response of the developmental (gametogenesis and sporogenesis) processes to nanoparticles (NPs) exposure, the aerial application of nZnO and their ionic counterpart of ZnSO4 at four different levels were examined on bean plants (Phaseolus vulgaris) before the flowering stage. To evaluate the mentioned processes, briefly, flowers in multiple sizes were fixed in paraffin, followed by sectioning and optical analysis. The possibility of alteration in reproductive cells was thoroughly analyzed using both light and electron microscopes. Overall, our results revealed the histological defects in male and female reproductive systems of mature plants depend on NPs levels. Furthermore, NPs caused tapetum abnormalities, aberrations in carbohydrate accumulation, and apoptosis. The nZnO induced abnormal alterations right after meiosis and partly hindered the microspore development, leading to infertile pollens. The seed yield and dry weight were reduced to 70 and 82% at 2,000 mg L-1 nZnO foliar exposure, respectively. The sodium dodecyl sulfate (SDS)-polyacrylamide gel electrophoresis pattern showed the increased expression of two proteins at the molecular weight of 28 and 42 kDa at various concentrations of nZnO and ZnSO4. Overall, our results provided novel insights into the negative effect of nano-scaled Zn on the differential mechanism involved in the reproductive stage of the plants compared with salt form.

Exogenous application of ZnO nanoparticles and ZnSO4 distinctly influence the metabolic response in Phaseolus vulgaris L.

Nanomaterials-mediated contamination (including the highly reactive metal oxides ZnO nanoparticles) is becoming one of the most concerning issues worldwide. In this study, the toxic effects of two chemical species of Zn (ZnO nanoparticles and bulk ZnSO4) were investigated in bean plants, following either foliar or soil application, at concentrations from 250 to 2000 mg L-1 using biochemical assays, proteomics and metabolomics. The accumulation of Zn in plant tissues depended on the application type, zinc chemical form and concentration, in turn triggering distinctive morphological, physiological, and redox responses. Bean plants were more sensitive to the foliar than to the soil application, and high concentrations of ZnO NP and bulk ZnSO4 determined the highest plant growth inhibition and stress symptoms. However, low dosages of ZnSO4 induced a slight plant growth promotion and better physiological and antioxidative response. Low concentration of Zn leaded to increased activity of stress-related proteins and secondary metabolites with antioxidant capacity, while increasing concentration reached the exhausted phase of the plant stress response, reducing the antioxidant defense system. Such high concentrations increased lipids peroxidation, protein degradation and membranes integrity. Oxidative damage occurred at high concentrations of both chemical species of Zn. Foliar spraying impaired photosynthetic efficiency, while soil applications (especially ZnSO4) elicited antioxidant metabolites and proteins, and impaired chloroplast-related proteins involved in the electron transport chain and ATP production. Taken together, the results highlighted distinctive and nanoparticles-related toxic effects of ZnO in bean, compared to ionic forms of Zn.

Proteomics Revealed Distinct Responses to Salinity between the Halophytes Suaeda maritima (L.) Dumort and Salicornia brachiata (Roxb).

Plant resistance to salinity stress is one of the main challenges of agriculture. The comprehension of the molecular and cellular mechanisms involved in plant tolerance to salinity can help to contrast crop losses due to high salt conditions in soil. In this study, Salicornia brachiata and Suaeda maritima, two plants with capacity to adapt to high salinity levels, were investigated at proteome level to highlight the key processes involved in their tolerance to NaCl. With this purpose, plants were treated with 200 mM NaCl as optimal concentration and 500 mM NaCl as a moderate stressing concentration for 14 days. Indeed, 200 mM NaCl did not result in an evident stress condition for both species, although photosynthesis was affected (with a general up accumulation of photosynthesis-related proteins in S. brachiata under salinity). Our findings indicate a coordinated response to salinity in both the halophytes considered, under NaCl conditions. In addition to photosynthesis, heat shock proteins and peroxidase, expansins, signaling processes, and modulation of transcription/translation were affected by salinity. Interestingly, our results suggested distinct mechanisms of tolerance to salinity between the two species considered, with S. brachiata likely having a more efficient mechanism of response to NaCl.

Relatively Low Dosages of CeO2 Nanoparticles in the Solid Medium Induce Adjustments in the Secondary Metabolism and Ionomic Balance of Bean (Phaseolus vulgaris L.) Roots and Leaves.

Nanoparticles (NPs) are known to significantly alter plant metabolism in a dose-dependent manner, with effects ranging from stimulation to toxicity. The metabolic adjustment and ionomic balance of bean (Phaseolus vulgaris L.) roots and leaves gained from plants grown in a solid medium added with relatively low dosages (0, 25, 50, and 100 mg/L) of CeO2 NPs were investigated. Ce accumulated in the roots (up to 287.91 mg/kg dry weight) and translocated to the aerial parts (up to 2.78% at the highest CeO2 dosage), and ionomic analysis showed that CeO2 NPs interfered with potassium, molybdenum, and zinc. Unsupervised hierarchical clustering analysis from metabolomic profiles suggested a dose-dependent and tissue-specific metabolic reprogramming induced by NPs. The majority of differential metabolites belonged to flavonoids and other phenolics, nitrogen-containing low molecules (such as alkaloids and glucosinolates), lipids, and amino acids.

Morphological, proteomic and metabolomic insight into the effect of cerium dioxide nanoparticles to Phaseolus vulgaris L. under soil or foliar application.

Chemically synthesized nanoparticles (NPs) are widely used in industry and concern over their impact on the environment is rising. In this study, greenhouse grown bean (Phaseolus vulgaris L.) plants were treated with CeO2 NPs suspensions at 0, 250, 500, 1000, and 2000mgL-1 either aerially by spraying or via soil application. At 15days after treatment, plants were analyzed for Ce uptake, morphological and biochemical assays, as well as high-resolution mass spectrometry based metabolomics and proteomics. The results from ICP-MS assays showed a dose dependent absorption, uptake and translocation of Ce through both roots and leaves; Ce content increased from 0.68 up to 1894mgkg-1 following spray application, while concentrations were three orders lower following soil application (0.59 to 2.19mgkg-1). Electrolyte leakage increased with NPs rate, from 25.2% to 70.3% and from 24.8% to 32.9% following spray and soil application, respectively. Spraying lowered stomatal density (from 337 to 113 per mm2) and increased stomatal length (from 12.8 to 19.4µm), and altered photosynthesis and electron transport chain biochemical machinery. The increase in Ce content induced accumulation of osmolites (proline increased from 0.54 to 0.65mg/g under spray application), phytosiderophores (muconate and mugineate compounds showed increase fold-changes >16) and proteins involved in folding or turnover. NPs application induced membrane damage, as evidenced by the increase in membrane lipids degradates and by the increase in electrolyte leakage, and caused oxidative stress. Most of the responses were not linear but dose-dependent, whereas metabolic disruption is expected at the highest NPs dosage. Both proteomics and metabolomics highlighted a stronger effect of CeO2 NPs spraying, as compared to soil application. High concentrations of NPs in the environment have been confirmed to pose toxicity concern towards plants, although important differences could be highlighted between aerial deposition and soil contamination.