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Adaptation and tolerance mechanisms developed by mycorrhizal Bipinnula fimbriata plantlets (Orchidaceae) in a heavy metal-polluted ecosystem

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Abstract

The adaptation and performance of orchid mycorrhizae in heavy metal-polluted soils have been poorly explored. In the present study, proteomic and metabolic approaches were used to detect physiological changes in orchid roots established in a heavy metal-polluted soil and to ascertain whether mycorrhizal fungi affect the metabolic responses of roots. Young Bipinnula fimbriata plantlets were established in control and heavy metal-polluted soils in a greenhouse. After 14 months, exudation of root organic acids, phenolics, percentage of mycorrhization, mineral content, and differential protein accumulation were measured. More root biomass, higher root colonization, and higher exudation rates of citrate, succinate, and malate were detected in roots growing in heavy metal-polluted soils. Higher accumulation of phosphorus and heavy metals was found inside mycorrhizal roots under metal stress. Under non-contaminated conditions, non-mycorrhizal root segments showed enhanced accumulation of proteins related to carbon metabolism and stress, whereas mycorrhizal root segments stimulated protein synthesis related to pathogen control, cytoskeleton modification, and sucrose metabolism. Under heavy metal stress, the proteome profile of non-mycorrhizal root segments indicates a lower induction of defense mechanisms, which, together with the stimulation of enzymes related to carotenoid biosynthesis and cell wall organization, may positively influence mycorrhizal fungi colonization. The results point to different metabolic strategies in mycorrhizal and non-mycorrhizal root segments that are exposed to heavy metal stress. The results indicate that root colonization by mycorrhizal fungi is stimulated to alleviate the negative effects of heavy metals in the orchids.

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Acknowledgements

The authors thank the Instituto Tecnológico Vale (Belem, Brazil) for equipment supply and technical assistance and Ira Fogel for editorial and English improvement. This work was supported by the ‘Fondo Nacional de Desarrollo Científico y Tecnológico’ of Chile [grant number 1170931 to C.A.] and the ‘Comisión Nacional de Investigación Científica y Tecnológica’ of Chile [grant number 21130491 to H.H.].

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Correspondence to Cesar Arriagada.

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This study is dedicated for the memory of the German/Spanish mycorrhizae researcher, Horst Vierheilig (1960–2011) of CSIC, Spain

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Fig. S1

Colonization percentage of 200 random peloton-containing root segments (~10 mm) of 5 Bipinnula fimbriata plants, estimated according to Schatz et al. (2010) (PNG 36 kb)

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Fig. S2

PCA analysis showing distribution of main protein clusters (PC) in Bipinnula fimbriata root segments (mycorrhizal and non-mycorrhizal) developed in control and heavy metal-polluted soil. PC1 = Ribosomal protein; PC2 = Copper transporter 6; PC3 = Epoxycarotenoid dioxygenase; PC4 = ATP synthase; PC5 = Peroxidase; PC6 = HSP70; PC7 = Actin; PC8 = Glyceraldehyde-3-phosphate dehydrogenase; PC9 = Sucrose synthase; PC10 = Glutamate decarboxylase; PC11 = Monodehydroascorbate reductase; PC12 = ATP synthase alpha subunit; PC13 = Ubiquitin-like protein; PC14 = Beta-tubulin; PC15 = Isoflavone reductase; PC16 = Catalase 1; PC17 = Profilin; PC18 = Allene oxide synthase; PC19 = Alpha-tubulin; PC20 = Orcinol O-methyltransferase; PC21 = LFY-like protein OrcLFY; PC22 = Lipoxygenase; PC23 = Knotted-like protein; PC24 = Phenylalanine ammonia lyase; PC25 = ATPase; PC26 = Hypothetical protein (related to ATP-binding cassette domain*); PC27 = S-adenosylmethionine synthetase; PC28 = V-ATPase E subunit; PC29 = 3-ketoacil-CoA thiolase; PC30 = Chalcone synthase; PC31 = Ascorbate peroxidase; PC32 = Ribulose-1,5-bisphosphate carboxylase/oxygenase; PC33 = Peptidyl-prolyl cis-trans isomerase;; PC34 = Ribosomal protein S3a. (PNG 357 kb)

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Herrera, H., Valadares, R., Oliveira, G. et al. Adaptation and tolerance mechanisms developed by mycorrhizal Bipinnula fimbriata plantlets (Orchidaceae) in a heavy metal-polluted ecosystem. Mycorrhiza 28, 651–663 (2018). https://doi.org/10.1007/s00572-018-0858-4

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