Jalal, da Silva Oliveira, Rosa, Galindo & Teixeira Filho 2023 — Plant growth-promoting microorganisms mitigating climatic-extreme abiotic stresses (narrative review)

This MDPI Life review synthesises laboratory, greenhouse, and field evidence on how plant growth-promoting rhizobacteria (PGPB, including Azospirillum, Bradyrhizobium, Pseudomonas, Bacillus, Enterobacter, Burkholderia, Pantoea, Rhizobium, Serratia, Arthrobacter, Microbacterium spp. and others) and plant growth-promoting fungi (PGPF, including arbuscular mycorrhizal fungi Glomus / Funneliformis / Rhizophagus, Trichoderma, Penicillium, Aspergillus spp.) ameliorate the impact of climatic-extreme abiotic stresses on cereal, legume, oilseed, vegetable, and forage crops. The abstract (page 1) groups the stresses into six categories — “drought, salinity, heavy metals, flooding, extreme temperatures, and intense light” — and the body splits “extreme temperatures” into separate high-temperature (Section 5) and low-temperature (Section 6) sections, yielding seven body chapters: drought, salinity, heavy metals, high temperature, low temperature, flooding/oxygen deficit, and intense light. The paper is a narrative review with no independent measurements, no primary data extraction, and no quantitative meta-analysis; tabular entries in Tables 1–3 are microorganism / stress / host-plant pairings catalogued from cited primary studies rather than occurrence values. It is ingested as an out-of-core-scope agronomic-mitigation-context reference following the asgher2023-selenium-heavy-metal-stress-plants and bae2018-absorbent-hygiene-pads-safety-review precedent for methodology / context reviews without primary metal-occurrence data; metals: [], ingredients: [], and products: [] are correct because the paper contributes no measured contamination values to any HMI ingredient, product, or metal page. The heavy-metals section (Section 4, pages 7–8, and Table 2) is potentially useful as a starting point for a future HMI mitigation-lever entry on microbial bioremediation / phytostabilisation / phytoextraction / phyto-volatilisation as a soil-side intervention to reduce heavy-metal uptake into crops, but each specific mechanistic or quantitative claim should be sourced from its underlying primary citation rather than from this tertiary review.

Key numbers

This is a narrative review with no primary measurements. The numerical content consists of (a) the review’s own qualitative framing of heavy-metal toxicity mechanisms, (b) microorganism × heavy-metal pairings catalogued from cited primary studies in Table 2, and (c) crop-yield / stress-impact statistics quoted from cited primary studies in the prose.

Author-stated framing of heavy metals (Section 4, pages 7–8)

• “Heavy metals are generally categorized to belong to the group of metals and metalloids with high atomic density (density greater than 4 g cm⁻³) and mass” (cited to ref [142], page 7).
• “Heavy metals include non-essential plant elements such as lead (Pb), cadmium (Cd), aluminum (Al), chromium (Cr), mercury (Hg), arsenic (As), silver (Ag), and platinum group elements” (cited to refs [143,146]).
• “Some heavy metals, such as copper (Cu), iron (Fe), manganese (Mn), zinc (Zn), nickel (Ni), and molybdenum (Mo), are essential micronutrients … however, their high concentration can cause phytotoxicity” (cited to refs [143,147]).
• “Heavy metal toxicity in plants can cause leaf chlorosis, alter chlorophyll a and b ratios, decrease photosynthesis, inhibit root elongation, increase ROS production and membrane leakage, and change lipid composition through changing inter-cellular concentrations of nutrients” (cited to refs [148,149], page 8).
• Microbe-mediated remediation modes listed: “Microbes play a key role in the remediation of HMs through phyto-stabilization, phyto-extraction, and phyto-volatilization” (cited to refs [131,146]).

Table 2 — Microorganism × heavy-metal pairings in contaminated-site remediation studies, 2010–2020 (page 8)

Microorganism / heavy metal / primary-citation reference, as catalogued by the authors. The review does not report concentration values; it reports which microbe was studied against which metal in which cited primary study.

Microbe-and-heavy-metal context bullets from prose (pages 7–8)

• Most-represented bacterial genera in heavy-metal-contaminated sites listed as Bacillus, Pseudomonas, and Arthrobacter in phyla Firmicutes, Proteobacteria, and Actinobacteria (cited to refs [131,151]).
• Microbial enhancement of phytoremediation attributed to organic-acid production, siderophore production, bio-surfactant production, bio-methylation, and redox processes that “transform heavy metals into soluble and bioavailable forms” (cited to refs [9,150]). Note the directionality: in a phytoextraction context, “bioavailable” means more uptake into plant shoots for harvest-and-disposal; in a food-safety context the same mechanism risks increased contamination of edible crop fractions. The review does not draw this distinction.
• IAA and ACC-deaminase synthesis by PGPB / PGPF cited as the molecular mechanisms enhancing biomass and phytoremediation under heavy-metal exposure (cited to refs [131,150]).
• Co-stress study: Farwell et al. inoculated canola with Pseudomonas putida UW4 under nickel and flood stress and reported increased canola growth and biomass under flooding + heavy-metal stress (cited to ref [250], page 12). Cao et al. reported that flooding “increased enzymatic activity in copper (Cu)-contaminated soil” and that Cu presence is “inversely proportional to soil microbiota (bacteria and fungi)” (cited to ref [239], page 12).

Author-stated crop / yield statistics from cited primary studies (Section 2–3, pages 5–6; not heavy-metals-specific)

• “Drought can reduce yield and cultivation potential (ideal yield) of soybean by up to 70%” (cited to ref [92], page 5).
• “Soils irrigated with saturated water extract with an EC of 4.0 dS m⁻¹ (40 mmol L⁻¹ of NaCl) are considered to be saline and can cause osmotic pressure of 0.2 MPa that leads to a reduction in vegetable yields” (cited to ref [119], page 6).
• These figures are reported here only because they appear in the source’s framing; they are not heavy-metals occurrence values and do not feed any wiki page.

Methods (brief)

Narrative literature review covering predominantly 2012–2022 with select earlier citations back to 2007. The authors did not declare a PRISMA protocol, did not report search platforms / databases / search strings, did not state inclusion or exclusion criteria, and did not perform quantitative meta-analysis or independent data extraction. The structure is a thematic synthesis organised by stress class (drought, salt, heavy metals, high temperature, low temperature, flooding, light). Tables 1–3 catalogue microorganism / stress / host-plant pairings from cited primary studies, listing only the microbe, the stress class, the plant species, and the primary citation — no concentrations, doses, durations, or quantitative response measurements are tabulated. Figures 1–2 are schematic diagrams of abiotic-stress impact pathways and microbe-induced resistance mechanisms, not quantitative data. The review reports no novel laboratory work, no independent re-analysis of primary data, and no occurrence measurements in any food, feed, soil, or environmental matrix.

Implications

• Certification (HMTc): This review contributes no occurrence values to any HMTc product-category threshold. It is potentially useful as background reading for an HMTc educational note on agronomic / soil-side mitigation levers (PGPB and PGPF inoculation, AMF co-application) that have been investigated as ways to reduce heavy-metal uptake into cereal, legume, and vegetable crops grown on contaminated soils. Any HMTc-side use of specific mechanistic claims should be traced through this review to the underlying primary references rather than cited from the review itself. The “bioavailable forms” framing in the review (refs [9,150]) is directionally ambiguous — phytoextraction strategies increase shoot bioavailability for harvest-and-disposal whereas food-safety strategies seek to decrease edible-fraction bioavailability; HMTc-side use must disambiguate.
• Courses: Useful as a reference for an educational module on soil-side mitigation levers — covering phyto-stabilisation, phyto-extraction, and phyto-volatilisation as three distinct microbe-assisted remediation modes (page 8, refs [131,146]); the role of IAA, ACC-deaminase, siderophores, and organic acids as microbial mechanisms; and the genera most-represented in heavy-metal-contaminated sites (Bacillus, Pseudomonas, Arthrobacter). The table provides a starting catalogue of microbe / metal / primary-reference combinations that course authors can trace back to primary studies.
• App: Not applicable. No per-product or per-ingredient occurrence values; no consumer-facing exposure estimates.
• Microbiome: Adjacent. The review’s heavy-metals section (Section 4 + Table 2) and the flood + Cu / Ni co-stress passages (Section 7, page 12) intersect microbiome-and-heavy-metals territory, but in the agronomic / rhizosphere register rather than the human-gut / WikiBiome federation register. Out of scope for microbiome federation as currently scoped; flag for the future agronomic-microbiome-and-heavy-metals page if one is created.
• Synthesis: No synthesis triggers fire from this ingest. The paper does not contribute primary occurrence values to any ingredient contamination_profile cell.

Wiki pages this source may touch

This is a narrative agronomic-mitigation review; it contributes context rather than primary data. Potential touch points for future synthesis or educational use (not generating routing rows because no occurrence data are reported):

• Mitigation-lever context for cereal ingredient pages where PGPB / PGPF / AMF inoculation has been studied as an uptake-reduction or phytostabilisation intervention (rice, wheat, maize, sorghum, foxtail millet, pearl millet, oat, barley).
• Mitigation-lever context for legume and oilseed ingredient pages (soybean, common bean, cowpea, chickpea, peanut, rapeseed/canola, safflower).
• Mitigation-lever context for vegetable ingredient pages (tomato, pepper, cucumber, lettuce, mustard, broccoli/cabbage Brassicaceae).
• Background reference for metals/cadmium, metals/lead, metals/arsenic, metals/chromium, metals/nickel, metals/copper, metals/zinc, and metals/mercury mitigation sections discussing microbe-assisted phytoremediation as a soil-side intervention.
• Reference for any future mitigation/pgpb-inoculation.md, mitigation/amf-coapplication.md, or mitigation/microbial-phytoextraction.md page.

Verification notes

• No primary occurrence data. metals: [], ingredients: [], and products: [] are correct. Following the asgher2023-selenium-heavy-metal-stress-plants precedent (and the earlier bae2018-absorbent-hygiene-pads-safety-review precedent for methodology / regulatory-context reviews without primary measurements): this paper reviews laboratory and field experiments on microbial mitigation of abiotic stresses in plants; it does not report contamination levels in any food ingredient or product. Routing to metal or ingredient pages as direct_evidence would mischaracterise the evidence. The mitigation-lever angle (PGPB / PGPF / AMF microbial inoculation reducing or modulating Cd / Pb / As / Cr / Ni / Cu / Zn accumulation in crops grown on contaminated soils) is documented in body text for future discoverability without generating misleading routing rows.
• Speciation discipline. The paper uses “As” inconsistently — Table 2 lists Sporosarcina ginsengisoli against “As(III)” (page 8) and Bacillus thuringiensis GDB-1 and the algal entries simply against “As” without speciating; the review also lists Cr(VI) for some entries and bare “Cr” elsewhere. The review does not analyse arsenic speciation in plant tissues post-treatment and does not separate MeHg from tHg. Because this page reports the review’s own framing without overlaying speciation distinctions the authors did not make, metals: [] avoids forcing a speciation choice the source does not support.
• Plant-tissue and soil matrices. matrices: [plant-tissue, soil] reflects that the experiments cited measure microbial activity and heavy-metal partitioning in plant material (roots, shoots, biomass) and in rhizosphere / contaminated soil, not in food as consumed.
• Phytoextraction-vs-food-safety directionality. The review’s “transform heavy metals into soluble and bioavailable forms” framing (page 8, refs [9,150]) reflects a phytoextraction perspective where increased shoot bioavailability is the desired outcome (harvest and remove the plant biomass to clean the soil). In a food-safety context the same mechanism is undesirable — increased uptake into the edible crop fraction. The review does not draw this distinction. Future synthesis work that touches this paper must disambiguate whether a cited primary study used the microbial inoculation to increase uptake (phytoextraction goal) or to decrease edible-fraction uptake (food-safety goal); the two framings imply opposite HMTc-side recommendations.
• Brand-firewall compliance (Part 12). No commercial product or brand names appear in the paper. Methods sections of cited primary studies are not reproduced at instrument-vendor level in this review. No Part 12 concerns.
• Wiki/HMTc firewall (Part 2) compliance. The page reports what the review describes (microbe-stress-plant pairings, mechanism framing, qualitative statements about phytoremediation modes) without proposing HMTc thresholds, endorsing the review’s synthesis claims as wiki consensus, or making consumer-audience risk statements. The crop-yield statistics quoted in prose (drought reducing soybean yield by up to 70%, salinity at EC 4.0 dS m⁻¹ reducing vegetable yield) are reported as what the review says, not adopted as wiki claim.
• Evidence tier. Tier B — peer-reviewed narrative review without PRISMA protocol, without reported search platforms or databases, and without independent meta-analysis. Per conventions evidence grading, narrative reviews sit below primary peer-reviewed studies (Tier A) but above grey literature; specific claims attributed in tables are no stronger than the underlying primary references they cite.
• Sample-size. sample_n: null is correct for a narrative review with no defined sample frame for evidence extraction.
• License. MDPI Life publishes under Creative Commons Attribution (CC BY 4.0) license per MDPI’s standard open-access policy. DOI 10.3390/life13051102 resolves to the open-access article. Copyright statement on page 1 confirms: ”© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license.”
• Funding statement (page 13): “This review received funding from The World Academy of Science (TWAS) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the first author’s doctoral fellowship (CNPq/TWAS grant number: 166331/2018-0) and the productivity research grant (award number 311308/2020-1) of the corresponding author.” “Conflicts of Interest: The authors declare no conflict of interest.”
• Audit subagent (2026-06-02) flagged Check 1 ⚠️ on the “high atomic density” citation, which the wiki page initially attributed to “[142,143]”; verified against PDF page 7 — the high-atomic-density sentence is cited to [142] only, with [143] attached to the following sentence (“The term HMs refers to any metallic element…”). Corrected to “[142]“. Audit also flagged Check 1 ⚠️ on the “seven climatic-extreme abiotic stresses” framing, noting the abstract groups the stresses into six categories; verified against pages 1 (abstract) vs Section 5 / Section 6 (body) — both framings are correct in different parts of the source. Lead paragraph revised to acknowledge both the abstract’s six-category grouping and the body’s seven-section structure rather than choosing one. Audit verdict was PROMOTE with no ❌ findings; both ⚠️ findings applied for accuracy polish.

Ingest log

• 2026-06-02 fresh ingest (Claude Opus 4.7, autonomous v2.0 manual-fetch skill, daemon tick): NEW path. Three identity checks against wiki/sources/ returned no hits: DOI 10.3390/life13051102 not present; raw_handle MFK_life-13-01102 not present; cite-key stem jalal2023 not present. PDF SHA-256 4ed843c1496521777731230f175e1450c8aa10697f55a98fc864aa704bf57ec6. Paper is a narrative review of plant growth-promoting microorganisms (bacteria and fungi) mitigating seven climatic-extreme abiotic stresses including heavy metals; no primary occurrence measurements. Ingested as out-of-core-scope agronomic-mitigation-context reference per the asgher2023-selenium-heavy-metal-stress-plants precedent; metals: [], ingredients: [], products: [] correctly reflect that no contamination values are contributed to any wiki page. Heavy-metals content captured: Section 4 framing (pages 7–8), Table 2 microbe × metal pairings (page 8), and the Farwell / Cao co-stress passages from Section 7 (page 12).

Page history

The five most recent substantive edits to this page. The full version history lives in git; when DOI minting comes online (see schema docs), each entry below will also link to a version-pinned DataCite DOI.