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Table 1 The toxic effect of HMs on filamentous pathogens

From: Fungal and oomycete pathogens and heavy metals: an inglorious couple in the environment

Metal

Pathogen group

Concentration

Species

Disease(s)

Effect(s)

References

Ag

Fungi

15 mg·L−1

Alternaria alternata

Leaf spot, black spot

- Growth inhibition

- Damage and deformation of hyphae and conidia

- Disorders in the total content of protein/lipids/sugar/n-acetyl glucosamine

Ouda (2014)

Botrytis cinerea

Gray mold

5–250 ppm

Sclerotinia sclerotiorum

White mold

- Growth inhibition

Mwangi et al. (2014)

Oomycetes

5–50 ppm

Phytophthora spp.

Soil- and water-borne plant pathogens

- Zoospore death

Slade and Pegg (1993)

Ba

Fungi

10–4 to 10–5 M

Alternaria solani

Early blight

- Inhibition of spore germination

- Inhibition of germ tube growth

Bhajbhuje (2013)

Cd

Fungi

10–4 to 10–5 M

Alternaria solani

Early blight

- Inhibition of spore germination

- Inhibition of germ tube growth

Bhajbhuje (2013)

200 mg·L−1

Aspergillus fumigatus

Aspergillosis

- Hyphae decolorisation

Mohammadian Fazli et al. (2015)

0.175–3.0 mM

Botrytis cinerea

Gray mold

- Growth inhibition

- Over-accumulation of hydrolases and oxidases

Cherrad et al. (2012)

100 ppm

Fusarium oxysporum

Fusarium wilt

- Growth inhibition

Golubović-Ćurguz (2010)

0.150 mM

Fusarium oxysporum

Fusarium wilt

- Acquisition orange tones of mycelium

Lorenzo-Gutiérrez et al. (2019)

0.1 mM

Heliscus lugdunensis (Neonectria lugdunensis)

Black foot

- Growth inhibition (50% decrease)

Jaeckel et al. (2005)

200 mg·L−1

Paecilomyces sp.

Oculomycosis

Pistachio dieback

Entomopathogenic species

- Hyphae decolorisation

Mohammadian Fazli et al. (2015)

50 μM

Phanerochaete chrysosporium

White-rot (woody plants) Granulomatous lung disease

- Oxidative stress induction

-Time-dependent up-regulation of CAT, POX, LiP, and MnP activities

Zhang et al. (2015)

1–500 μM

Phanerochaete chrysosporium

White-rot (woody plants) Granulomatous lung disease

- Viability reduction

- CAT activity up-regulation

Chen et al. (2014)

0.1 mM

Rhizopus arrhizus

Rhizopus soft rot mucormycosis

- Reduction in hyphae length

- Reduction in the number of branches

Gadd et al. (2001)

0.1–0.2 mM

Schizophyllum commune

Sap rot, Schizophyllum rot fungal sinusitis

- Inhibition of radial growth

Lilly et al. (1992)

5–250 ppm

Sclerotinia sclerotiorum

White mold

- Growth inhibition

Mwangi et al. (2014)

1, 5 and 10 mmol/L

Trichosporon cutaneum

White piedra

- SOD activity up-regulation

Lazarova et al. (2014)

0.7 mM

Verticillium cf. alboatrum

Verticillium wilt

- Growth inhibition (30% decrease)

Jaeckel et al. (2005)

Oomycetes

0.05–3.0 mM

Achlya bisexualis

Saprolegniasis in fishes

- Decrease in mycelial area and radial extension

Lundy et al. (2001)

5 and 12.5 mg/L

Phytophthora infestans

Late blight

- ROS and RNS formation

- Increase in protein carbonylation content

- Up-regulation of CAT and SOD activities

- Nitro-oxidative modifications of proteins and nucleic acids

Gajewska et al. (2020)

10–50 µg/ml

Saprolegnia delica Coker

Saprolegniasis in fishes

- Inhibition of sporangia formation

- Morphological abnormality (e.g. thicker and stunted vegetative hyphae, shorter and thicker zoosporangia, low numbers of oogonia and antheridia)

Ali (2007)

Cu

Fungi

25–100 ppm

Alternaria alternata

Leaf spot, black spot

- Increase in total protein content

- CAT activity up-regulation

Shoaib et al. (2015)

15 mg·L−1

Alternaria alternata

Leaf spot, black spot

- Growth inhibition

- Damage and deformation of hyphae and conidia

- Disorders in the total content of protein, lipids, sugar and n-acetyl glucosamine

Ouda (2014)

10–4 to 10–5 M

Alternaria solani

Early blight

- Inhibition of spore germination

- Inhibition of germ tube growth

Bhajbhuje (2013)

0.5 mM

Aspergillus niger

Black mold

- Growth inhibition

- Nitrate-dependent induction of oxalic acid production

Sazanova et al. (2015)

20 and 40 ppm

Aspergilus niger

Black mold

Pneumonia

- Growth inhibition

- Decrease in the colony numbers

Abu-Mejdad (2013)

15 mg·L−1

Botrytis cinerea

Gray mold

- Growth inhibition

- Damage and deformation of hyphae and conidia

- Disorders in the total content of protein, lipids, sugar and n-acetyl glucosamine

Ouda (2014)

0.5 mM

Penicillium citrinum

Yellow rice disease (citrinin production) a tissue-invasive cause of pneumonia

- Growth inhibition

- Nitrate-dependent induction of oxalic acid production

Sazanova et al. (2015)

0.1 mM

Rhizopus arrhizus

Rhizopus soft rot mucormycosis

- Reduction of hyphae length

- Reduction in the number of branches

Gadd et al. (2001)

1, 5, 3 mmol/L

Trichosporon cutaneum

White piedra

- Oxidative stress induction

- SOD activity up-regulation

Lazarova et al. (2014)

Oomycetes

0.05–3.0 mM

Achlya bisexualis

Saprolegniasis in fishes

- Decrease in mycelial area and radial extension

Lundy et al. (2001)

0.5–1 mM

Phytophthora capsici

Blight and fruit rot of peppers

- Growth inhibition

- Limited sporulation

Liu et al. (2018)

Co

Oomycetes

0.05–3.0 mM

Achlya bisexualis

Saprolegniasis in fishes

- Decrease in mycelial area and radial extension

Lundy et al. (2001)

Cr

Fungi

10–4 to 10–5 M

Alternaria solani

Early blight

- Inhibition of spore germination

- Inhibition of germ tube growth

Bhajbhuje (2013)

1, 5 and 10 mmol/L

Trichosporon cutaneum

White piedra

- Oxidative stress induction

- SOD activity up-regulation

Lazarova et al. (2014)

Oomycetes

0.5–1 mM

Phytophthora capsici

Blight and fruit rot of peppers

- Growth inhibition

- Limited sporulation

Liu et al. (2018)

Fe

Fungi

10–4 to 10–5 M

Alternaria solani

Early blight

- Inhibition of spore germination

- Inhibition of germ tube growth

Bhajbhuje (2013)

Hg

Fungi

10–4 to 10–5 M

Alternaria solani

Early blight

- Inhibition of spore germination

- Inhibition of germ tube growth

Bhajbhuje (2013)

5–250 ppm

Sclerotinia sclerotiorum

White mold

- Growth inhibition

Mwangi et al. (2014)

Oomycetes

3 mM

Achlya bisexualis

Saprolegniasis in fishes

- Decrease in mycelial area and radial extension

- Spiral growth of hyphae

Lundy et al. (2001)

0.5–1 mM

Phytophthora capsici

Blight and fruit rot of peppers

- Growth inhibition

- Limited sporulation

Liu et al. (2018)

1 ppm

Phytophthora nicotianae var. parasitica

Black shank

- Reduction in zoospore germination

Slade and Pegg (1993)

Li

Oomycetes

1 ppm

Phytophthora nicotianae var. parasitica

Black shank

- Reduction in zoospore germination

Slade and Pegg (1993)

Mn

Oomycetes

0.1–200 mg/L

Phytophthora nicotianae

Black shank

- Growth inhibition

- Sporangiogenesis and zoosporogenesis inhibition

- Spores germination inhibition

- Concentration-dependent regulation of SOD and CAT activity

- Increased MDA content with increasing HM concentration

Luo et al. (2020)

Pb

Fungi

25 μM

Phanerochaete chrysosporium

White-rot (woody plants) Granulomatous lung disease

- ROS formation

- Time-dependent up-regulation of CAT, POD, LiP and MnP activities

Zhang et al. (2015)

Oomycetes

1 ppm

Phytophthora nicotianae var. parasitica

Black shank

- Reduction in zoospore germination

Slade and Pegg (1993)

10–50 µg/ml

Saprolegnia delica Coker

Saprolegniasis in fishes

- Inhibition of sporangia formation

- Morphological abnormality (e.g. thicker and stunted vegetative hyphae, shorter and thicker zoosporangia, low numbers of oogonia and antheridia)

Ali (2007)

Sr

Oomycetes

30 mM

Phytophthora cinnamomi

Root rot and cankering

- Encystment 90% of zoospores

Byrt et al. (1982)

Zn

Fungi

20 and 40 ppm

Aspergilus niger

Black mold

- Growth inhibition

- Decrease in the colony numbers

Abu-Mejdad (2013)

2 mM

Aspergillus niger

Black mold

- Growth inhibition

- Nitrate-dependent induction of oxalic acid production

Sazanova et al. (2015)

1–10 mM

Penicillium spp.

Allergic pulmonary disease

- Secretion a yellow substance related to the HM stress

Ezzouhri et al. (2009)

2 mM

Penicillium citrinum

Yellow rice disease (citrinin production) a tissue-invasive cause of Pneumonia

- Growth inhibition

- Nitrate-dependent induction of oxalic acid production

Sazanova et al. (2015)

0.1 mM

Rhizopus arrhizus

Mucormycosis

- Reduction of hyphae length

- Reduction in the number of branches

Gadd et al. (2001)

5–250 ppm

Sclerotinia sclerotiorum

White mold

- Growth inhibition

Mwangi et al. (2014)

Oomycetes

0.05–3.0 mM

Achlya bisexualis

Saprolegniasis in fishes

- Decrease in mycelial area and radial extension

Lundy et al. (2001)

0.1–20 mg/L

Phytophthora nicotianae

Black shank

- Growth inhibition

- Sporangiogenesis and zoosporogenesis inhibition

- Spores germination inhibition

- Concentration-dependent regulation of SOD and CAT activity

- Increased MDA content with Increasing HM concentration

Luo et al. (2020)