Element profiles and growth in Zn-sensitive and Zn-resistant Suilloid fungi

Colpaert, Jan; Adriaensen, Kristin; Muller, Ludo A. H.; Lambaerts, Marc; Faes, Christel; Carleer, Robert; Vangronsveld, Jaco

doi:10.1007/s00572-005-0009-6

Cited by 36 publications

(16 citation statements)

References 43 publications

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“…We showed S. luteus Zn tolerance phenotype to be negatively correlated with intracellular Zn accumulation. No outlier isolates were detected suggesting all individuals to use a similar detoxification strategy based on Zn exclusion as previously demonstrated by Colpaert et al (2005). The correlation between SlZnT2 transcript level and Zn tolerance phenotype that we demonstrated in 30 randomly selected S. luteus isolates might indicate a role for SlZnT2 in Zn export.…”

Section: Discussionsupporting

confidence: 77%

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Adaptive zinc tolerance is supported by extensive gene multiplication and differences in cis-regulation of a CDF transporter in an ectomycorrhizal fungus

Ruytinx

Coninx

Beeck

et al. 2019

Preprint

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16 17 Running title: Molecular genetic mechanisms of Zn tolerance in Suillus 18 2 Originality -significance statement 19To the best of our knowledge, this is the first study linking genotypes to adaptive phenotypes in 20 mycorrhizal fungi. It is unique in the way it combines evolutionary and functional genetics to allow 21 a significant advance in the understanding of responses to environmental stress factors in general 22 and, to soil metal pollution in particular. A better understanding of adaptive tolerance mechanisms 23 in keystone symbiotic fungi is paramount for developing impactful phyto and mycoremediation 24 strategies for metal polluted waste land and to predict the impact of future environmental change 25 on mycorrhizal diversity and ecosystem functioning. 26 3 Summary 27 Abiotic changes due to anthropogenic activities affect selection regimes for organisms. How trees 28 and their mycorrhizal symbionts adapt to altered environments in heterogeneous landscapes is of 29 great interest. With a global distribution and multiple adaptive phenotypes available, Suillus luteus 30 is an excellent ectomycorrhizal model to study evolutionary dynamics of local adaptation. We 31 assessed pathways of homeostasis and detoxification in S. luteus isolates, displaying contrasting 32 Zn tolerance phenotypes to identify mechanisms underlying adaptive Zn tolerance. Using 30 33 randomly selected isolates sampled at metal contaminated and control sites, we documented Zn 34 tolerance phenotypes, assessed the link with identified candidate genes and explored its genetic 35 basis via targeted amplicon sequencing and qPCR. Zn tolerance phenotypes covering a continuum 36 from Zn sensitive to hypertolerant were identified and inversely correlate with cellular Zn 37 accumulation. Gene expression of SlZnT2, encoding a putative Zn transporter explains 72% of the 38 observed phenotypic variation. SlZnT2 copy number varies among isolates and different promotor 39 genotypes were identified. Rapid adaptation in this species is supported by the cumulative effect of 40 gene copy number variation and differences in cis-regulation and might be triggered by 41 environmental stress rather than being the result of standing variation. 42 43 Keywords 44 Cation Diffusion Facilitator, Copy Number Variation, environmental adaptation, gene expression, 45 mycorrhiza, Suillus, zinc 46 69 al., 2004; Colpaert et al., 2011). Adaptive phenotypes of these species presumably support the 70 establishment of pines on severely contaminated soils (Colpaert et al., 2011). Evolutionary 71 dynamics of local adaptation and the genomic features governing the adaptive potential of these 72 particular Suilloid species are as for other ectomycorrhizal fungi not yet explored despite their 73 putative importance for the understanding of pine establishment on waste lands.74 Rapid adaptation to strong human induced shifts in the environment is repeatedly linked to discrete 75 traits. Discrete traits are traits with only a few possible phenotypes, clearly falling in discrete ...

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Section: Discussionsupporting

confidence: 77%

“…Lyophilized mycelia exposed to 1.5 mM Zn were acid digested (HNO 3 /HCl) (Colpaert et al, 2005) and mycelial Zn concentrations were analysed by inductively coupled plasma optical emission spectrometry (ICP-OES).…”

Section: Methodsmentioning

confidence: 99%

Adaptive zinc tolerance is supported by extensive gene multiplication and differences in cis-regulation of a CDF transporter in an ectomycorrhizal fungus

Ruytinx

Coninx

Beeck

et al. 2019

Preprint

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“…The former fungi can keep up growth and nutrient uptake and they reduce Zn and Cd transfer to their host. Analyses of element profiles of Zn and Cd‐tolerant S. luteus showed that the tolerance mechanism is largely based on Zn and Cd exclusion mechanisms (Colpaert et al. , 2005; Krznaric et al.…”

Section: Discussionmentioning

confidence: 99%

Zn pollution counteracts Cd toxicity in metal‐tolerant ectomycorrhizal fungi and their host plant, Pinus sylvestris

Krznaric¹,

Wevers²,

Cloquet³

et al. 2010

Environmental Microbiology

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SummaryAdaptive Zn and Cd tolerance have evolved in populations of the ectomycorrhizal fungus Suillus luteus. When exposed to high concentrations of both metals in vitro, a one-sided antagonism was apparent in the Zn-and Cd-tolerant isolates. Addition of high Zn concentrations restored growth of Cd-stressed isolates, but not vice versa. The antagonistic effect was not detected in a S. luteus isolate from non-contaminated land and in Paxillus involutus. The fungi were inoculated on pine seedlings and subsequently exposed to ecologically relevant Zn and Cd concentrations in single and mixed treatments. The applied doses severely reduced nutrient acquisition of nonmycorrhizal pines and pines inoculated with metalsensitive S. luteus. Highest translocation of Zn and Cd to shoots occurred in the same plants. Seedlings inoculated with fungi collected from the polluted site reduced metal transfer to their host and maintained nutrient acquisition under high metal exposure. The isolate showing highest tolerance in vitro also offered best protection in symbiosis. The antagonistic effect of high Zn on Cd toxicity was confirmed in the plant experiment. The results indicate that a Zn-and Cd-polluted soil has selected ectomycorrhizal fungi that are able to survive and protect their phytobiont from nutrient starvation and excessive metal uptake.

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“…The uptake of Cu and Cd by plants was also significantly reduced in mycorrhizal plants compared with that in non‐mycorrhizal ones. Similar results were also reported with other ectomycorrhizal fungi where metal transfer to the host was significantly reduced (Colpaert et al ., ; Krznaric et al ., ). Understanding the molecular‐based mechanism of heavy metal tolerance in the symbiotic system could aid the selection of the most efficient ectomycorrhizal isolates and plant fungus combinations for bioremediation and soil protection purposes.…”

Section: Discussionmentioning

confidence: 99%

Metal induction of aPisolithus albusmetallothionein and its potential involvement in heavy metal tolerance during mycorrhizal symbiosis

Reddy

Kour

Aggarwal

et al. 2016

Environmental Microbiology

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Metallothioneins (MTs) are small, cysteine-rich peptides involved in intracellular sequestration of heavy metals in eukaryotes. We examined the role in metal homeostasis and detoxification of an MT from the ectomycorrhizal fungus Pisolithus albus (PaMT1). PaMT1 encodes a 35 amino acid-long polypeptide, with 7 cysteine residues; most of them part of a C-x-C motif found in other known basidiomycete MTs. The expression levels of PaMT1 increased as a function of increased external Cu and Cd concentrations and were higher with Cu than with Cd. Heterologous complementation assays in metal-sensitive yeast mutants indicated that PaMT1 encodes a polypeptide capable of conferring higher tolerance to both Cu and Cd. Eucalyptus tereticornis plantlets colonized with P. albus grown in the presence of Cu and Cd showed better growth compared with those with non-mycorrhizal plants. Higher PaMT1 expression levels were recorded in mycorrhizal plants grown in the presence of Cu and Cd compared with those in control mycorrhizal plants not exposed to heavy metals. These data provide the first evidence to our knowledge that fungal MTs could protect ectomycorrhizal fungi from heavy metal stress and in turn help the plants to establish in metal-contaminated sites.

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Element profiles and growth in Zn-sensitive and Zn-resistant Suilloid fungi

Cited by 36 publications

References 43 publications

Adaptive zinc tolerance is supported by extensive gene multiplication and differences in cis-regulation of a CDF transporter in an ectomycorrhizal fungus

Adaptive zinc tolerance is supported by extensive gene multiplication and differences in cis-regulation of a CDF transporter in an ectomycorrhizal fungus

Zn pollution counteracts Cd toxicity in metal‐tolerant ectomycorrhizal fungi and their host plant, Pinus sylvestris

Metal induction of aPisolithus albusmetallothionein and its potential involvement in heavy metal tolerance during mycorrhizal symbiosis

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