An official website of the United States government
Zinc (Zn) is a plant essential micronutrient involved in a wide range of cellular processes. Ectomycorrhizal fungi (EMF) are known to play a critical role in regulating plant Zn status. However, how EMF control uptake and translocation of Zn and other nutrients in plant roots under different Zn conditions is not well known. Using X-ray fluorescence imaging, we found the EMF species Suillus luteus increased pine root Zn acquisition under low Zn concentrations and reduced its accumulation under higher Zn levels. By contrast, non-mycorrhizal pine roots exposed to high Zn indiscriminately take up and translocate Zn to root tissues, leading to Zn stress. Regardless of S. luteus inoculation, the absorption pattern of Ca and Cu was similar to Zn. Compared to Ca and Cu, effects of S. luteus on Fe acquisition were more marked, leading to a negative association between Zn addition and Fe concentration within EMF roots. Besides, higher nutrient accumulation in the fungal sheath, compared to hyphae inhabiting between intercellular space of cortex cells, implies the fungal sheath serves as a barrier to regulate nutrient transportation into fungal Hartig net. Our results demonstrate the crucial roles EMF play in plant nutrient uptake and how fungal partners ameliorate soil chemical conditions either by increasing or decreasing element uptake.
more »
« less
Comparative transcriptomics provides insights into molecular mechanisms of zinc tolerance in the ectomycorrhizal fungus Suillus luteus
Abstract Zinc (Zn) is a major soil contaminant and high Zn levels can disrupt growth, survival, and reproduction of fungi. Some fungal species evolved Zn tolerance through cell processes mitigating Zn toxicity, although the genes and detailed mechanisms underlying mycorrhizal fungal Zn tolerance remain unexplored. To fill this gap in knowledge, we investigated the gene expression of Zn tolerance in the ectomycorrhizal fungus Suillus luteus. We found that Zn tolerance in this species is mainly a constitutive trait that can also be environmentally dependent. Zinc tolerance in S. luteus is associated with differences in the expression of genes involved in metal exclusion and immobilization, as well as recognition and mitigation of metal-induced oxidative stress. Differentially expressed genes were predicted to be involved in transmembrane transport, metal chelation, oxidoreductase activity, and signal transduction. Some of these genes were previously reported as candidates for S. luteus Zn tolerance, while others are reported here for the first time. Our results contribute to understanding the mechanisms of fungal metal tolerance and pave the way for further research on the role of fungal metal tolerance in mycorrhizal associations.
more »
« less
- Award ID(s):
- 2029168
- PAR ID:
- 10572494
- Editor(s):
- Rokas, A
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- G3: Genes, Genomes, Genetics
- Volume:
- 14
- Issue:
- 9
- ISSN:
- 2160-1836
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Summary Arbuscular mycorrhizal fungi help their host plant in the acquisition of nutrients, and this association is itself impacted by soil nutrient levels. High phosphorus levels inhibit the symbiosis, whereas high nitrogen levels enhance it. The genetic mechanisms regulating the symbiosis in response to soil nutrients are poorly understood. Here, we characterised the symbiotic phenotypes in fourMedicago truncatula Tnt1‐insertion mutants affected in arbuscular mycorrhizal colonisation. We located theirTnt1insertions and identified alleles for two genes known to be involved in mycorrhization,RAM1andKIN3. We compared the effects of thekin3‐2andram1‐4mutations on gene expression, revealing that the two genes alter the expression of overlapping but not identical gene sets, suggesting thatRAM1acts upstream ofKIN3.Additionally,KIN3appears to be involved in the suppression of plant defences in response to the fungal symbiont.KIN3is located on the endoplasmic reticulum of arbuscule‐containing cortical cells, andkin3‐2mutants plants hosted significantly fewer arbuscules than the wild type.KIN3plays an essential role in the symbiotic response to soil nitrogen levels, as, contrary to wild‐type plants, thekin3‐2mutant did not exhibit increased root colonisation under high nitrogen.more » « less
-
Summary Stress is ubiquitous and disrupts homeostasis, leading to damage, decreased fitness, and even death. Like other organisms, mycorrhizal fungi evolved mechanisms for stress tolerance that allow them to persist or even thrive under environmental stress. Such mechanisms can also protect their obligate plant partners, contributing to their health and survival under hostile conditions. Here we review the effects of stress and mechanisms of stress response in mycorrhizal fungi. We cover molecular and cellular aspects of stress and how stress impacts individual fitness, physiology, growth, reproduction, and interactions with plant partners, along with how some fungi evolved to tolerate hostile environmental conditions. We also address how stress and stress tolerance can lead to adaptation and have cascading effects on population‐ and community‐level diversity. We argue that mycorrhizal fungal stress tolerance can strongly shape not only fungal and plant physiology, but also their ecology and evolution. We conclude by pointing out knowledge gaps and important future research directions required for both fully understanding stress tolerance in the mycorrhizal context and addressing ongoing environmental change.more » « less
-
Zinc ion (Zn 2+ ) is an essential micronutrient and a potent antioxidant. However, Zn 2+ is often limited in the environment. Upon Zn 2+ limitation, Mycolicibacterium (basonym: Mycobacterium ) smegmatis (Msm) undergoes a morphogenesis, which relies on alternative ribosomal proteins (AltRPs); i.e., Zn 2+ -independent paralogues of Zn 2+ -dependent ribosomal proteins. However, the underlying physiological changes triggered by Zn 2+ limitation and how AltRPs contribute to these changes were not known. In this study, we expand the knowledge of mechanisms utilized by Msm to endure Zn 2+ limitation, by comparing the transcriptomes and proteomes of Zn 2+ -limited and Zn 2+ -replete Msm . We further compare, corroborate and contrast our results to those reported for the pathogenic mycobacterium, M. tuberculosis , which highlighted conservation of the upregulated oxidative stress response when Zn 2+ is limited in both mycobacteria. By comparing the multi-omics analysis of a knockout mutant lacking AltRPs (Δ altRP ) to the Msm wild type strain, we specify the involvement of AltRPs in the response to Zn 2+ limitation. Our results show that AltRP expression in Msm does not affect the conserved oxidative stress response during Zn 2+ limitation observed in mycobacteria, but AltRPs do significantly impact expression patterns of numerous genes that may be involved in morphogenesis or other adaptive responses. We conclude that AltRPs are not only important as functional replacements for their Zn 2+ -dependent paralogues; they are also involved in the transcriptomic response to the Zn 2+ -limited environment.more » « less
-
Abstract Our understanding of the mechanisms mediating the resilience of organisms to environmental change remains lacking. Heavy metals negatively affect processes at all biological scales, yet organisms inhabiting contaminated environments must maintain homeostasis to survive. Tar Creek in Oklahoma, USA, contains high concentrations of heavy metals and an abundance of Western mosquitofish (Gambusia affinis), though several fish species persist at lower frequency. To test hypotheses about the mechanisms mediating the persistence and abundance of mosquitofish in Tar Creek, we integrated ionomic data from seven resident fish species and transcriptomic data from mosquitofish. We predicted that mosquitofish minimize uptake of heavy metals more than other Tar Creek fish inhabitants and induce transcriptional responses to detoxify metals that enter the body, allowing them to persist in Tar Creek at higher density than species that may lack these responses. Tar Creek populations of all seven fish species accumulated heavy metals, suggesting mosquitofish cannot block uptake more efficiently than other species. We found population‐level gene expression changes between mosquitofish in Tar Creek and nearby unpolluted sites. Gene expression differences primarily occurred in the gill, where we found upregulation of genes involved with lowering transfer of metal ions from the blood into cells and mitigating free radicals. However, many differentially expressed genes were not in known metal response pathways, suggesting multifarious selective regimes and/or previously undocumented pathways could impact tolerance in mosquitofish. Our systems‐level study identified well characterized and putatively new mechanisms that enable mosquitofish to inhabit heavy metal‐contaminated environments.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/g3journal/jkae156
