, Volume 28, Issue 7, pp 651–663 | Cite as

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

  • Héctor Herrera
  • Rafael Valadares
  • Guilherme Oliveira
  • Alejandra Fuentes
  • Leonardo Almonacid
  • Sidney Vasconcelos do Nascimento
  • Yoav Bashan
  • Cesar ArriagadaEmail author
Original Article


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.


Orchid mycorrhiza Organic acid exudation Proteome Contaminated soil 



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.].

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

572_2018_858_MOESM1_ESM.docx (32 kb)
ESM 1 (DOCX 31 kb)
572_2018_858_Fig3_ESM.png (36 kb)
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)

572_2018_858_MOESM2_ESM.tif (503 kb)
High Resolution Image (TIF 503 kb)
572_2018_858_Fig4_ESM.png (358 kb)
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)

572_2018_858_MOESM3_ESM.tif (1.2 mb)
High Resolution Image (TIF 1201 kb)
572_2018_858_MOESM4_ESM.xlsx (6.3 mb)
ESM 2 (XLSX 6478 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Héctor Herrera
    • 1
  • Rafael Valadares
    • 2
  • Guilherme Oliveira
    • 2
  • Alejandra Fuentes
    • 1
  • Leonardo Almonacid
    • 1
  • Sidney Vasconcelos do Nascimento
    • 2
  • Yoav Bashan
    • 3
    • 4
    • 5
  • Cesar Arriagada
    • 1
    Email author
  1. 1.Laboratorio de Biorremediación, Facultad de Ciencias Agropecuarias y Forestales, Departamento de Ciencias ForestalesUniversidad de La FronteraTemucoChile
  2. 2.Instituto Tecnologico ValeBelémBrazil
  3. 3.The Bashan Institute of ScienceAuburnUSA
  4. 4.Department of Entomology and Plant Pathology, 301 Funchess HallAuburn UniversityAuburnUSA
  5. 5.Environmental Microbiology Group, Northwestern Center for Biological Research (CIBNOR)La PazMexico

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