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Title: Fungal Endophyte Alternaria tenuissima Can Affect Growth and Selenium Accumulation in Its Hyperaccumulator Host Astragalus bisulcatus

Abstract

Endophytes can enhance plant stress tolerance by promoting growth and affecting elemental accumulation, which may be useful in phytoremediation. In earlier studies, up to 35% elemental selenium (Se 0) was found in Se hyperaccumulator Astragalus bisulcatus. Since Se 0 can be produced by microbes, the plant Se 0 was hypothesized to be microbe-derived. Here we characterize a fungal endophyte of A. bisulcatus named A2. It is common in seeds from natural seleniferous habitat containing 1,000–10,000 mg kg -1 Se. We identified A2 as Alternaria tenuissima via 18S rRNA sequence analysis and morphological characterization. X-ray microprobe analysis of A. bisulcatus seeds that did or did not harbor Alternaria, showed that both contained >90% organic seleno-compounds with C-Se-C configuration, likely methylselenocysteine and glutamyl-methylselenocysteine. The seed Se was concentrated in the embryo, not the seed coat. X-ray microprobe analysis of A2 in pure culture showed the fungus produced Se 0 when supplied with selenite, but accumulated mainly organic C-Se-C compounds when supplied with selenate. A2 was completely resistant to selenate up to 300 mg L -1, moderately resistant to selenite (50% inhibition at ~50 mg Se L -1), but relatively sensitive to methylselenocysteine and to Se extracted from A. bisulcatus (50% inhibition atmore » 25 mg Se L -1). Four-week old A. bisulcatus seedlings derived from surface-sterilized seeds containing endophytic Alternaria were up to threefold larger than seeds obtained from seeds not showing evidence of fungal colonization. When supplied with Se, the Alternaria-colonized seedlings had lower shoot Se and sulfur levels than seedlings from uncolonized seeds. In conclusion, A. tenuissima may contribute to the Se 0 observed earlier in A. bisulcatus, and affect host growth and Se accumulation. A2 is sensitive to the Se levels found in its host’s tissues, but may avoid Se toxicity by occupying low-Se areas (seed coat, apoplast) and converting plant Se to non-toxic Se 0. These findings illustrate the potential for hyperaccumulator endophytes to affect plant properties relevant for phytoremediation. Facultative endophytes may also be applicable in bioremediation and biofortification, owing to their capacity to turn toxic inorganic forms of Se into non-toxic or even beneficial, organic forms with anticarcinogenic properties.« less

Authors:
 [1];  [2];  [3];  [2];  [4];  [1]
  1. Colorado State Univ., Fort Collins, CO (United States). Dept. of Biology
  2. Laramie County Community College, Cheyenne, WY (United States). Dept. of Biology
  3. Colorado State Univ., Fort Collins, CO (United States). Dept. of Biology; Texas A & M Univ., San Antonio, TX (United States). Dept. of Sciences and Mathematics
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF); National Inst. of Health (NIH) (United States)
OSTI Identifier:
1477406
Grant/Contract Number:  
AC02-05CH11231; IOS-0817748; P20 RR016474
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; hyperaccumulation; selenium; endophyte; Alternaria; Astragalus; x-ray analysis

Citation Formats

Lindblom, Stormy D., Wangeline, Ami L., Valdez Barillas, Jose R., Devilbiss, Berthal, Fakra, Sirine C., and Pilon-Smits, Elizabeth A. H. Fungal Endophyte Alternaria tenuissima Can Affect Growth and Selenium Accumulation in Its Hyperaccumulator Host Astragalus bisulcatus. United States: N. p., 2018. Web. doi:10.3389/fpls.2018.01213.
Lindblom, Stormy D., Wangeline, Ami L., Valdez Barillas, Jose R., Devilbiss, Berthal, Fakra, Sirine C., & Pilon-Smits, Elizabeth A. H. Fungal Endophyte Alternaria tenuissima Can Affect Growth and Selenium Accumulation in Its Hyperaccumulator Host Astragalus bisulcatus. United States. doi:10.3389/fpls.2018.01213.
Lindblom, Stormy D., Wangeline, Ami L., Valdez Barillas, Jose R., Devilbiss, Berthal, Fakra, Sirine C., and Pilon-Smits, Elizabeth A. H. Mon . "Fungal Endophyte Alternaria tenuissima Can Affect Growth and Selenium Accumulation in Its Hyperaccumulator Host Astragalus bisulcatus". United States. doi:10.3389/fpls.2018.01213. https://www.osti.gov/servlets/purl/1477406.
@article{osti_1477406,
title = {Fungal Endophyte Alternaria tenuissima Can Affect Growth and Selenium Accumulation in Its Hyperaccumulator Host Astragalus bisulcatus},
author = {Lindblom, Stormy D. and Wangeline, Ami L. and Valdez Barillas, Jose R. and Devilbiss, Berthal and Fakra, Sirine C. and Pilon-Smits, Elizabeth A. H.},
abstractNote = {Endophytes can enhance plant stress tolerance by promoting growth and affecting elemental accumulation, which may be useful in phytoremediation. In earlier studies, up to 35% elemental selenium (Se0) was found in Se hyperaccumulator Astragalus bisulcatus. Since Se0 can be produced by microbes, the plant Se0 was hypothesized to be microbe-derived. Here we characterize a fungal endophyte of A. bisulcatus named A2. It is common in seeds from natural seleniferous habitat containing 1,000–10,000 mg kg-1 Se. We identified A2 as Alternaria tenuissima via 18S rRNA sequence analysis and morphological characterization. X-ray microprobe analysis of A. bisulcatus seeds that did or did not harbor Alternaria, showed that both contained >90% organic seleno-compounds with C-Se-C configuration, likely methylselenocysteine and glutamyl-methylselenocysteine. The seed Se was concentrated in the embryo, not the seed coat. X-ray microprobe analysis of A2 in pure culture showed the fungus produced Se0 when supplied with selenite, but accumulated mainly organic C-Se-C compounds when supplied with selenate. A2 was completely resistant to selenate up to 300 mg L-1, moderately resistant to selenite (50% inhibition at ~50 mg Se L-1), but relatively sensitive to methylselenocysteine and to Se extracted from A. bisulcatus (50% inhibition at 25 mg Se L-1). Four-week old A. bisulcatus seedlings derived from surface-sterilized seeds containing endophytic Alternaria were up to threefold larger than seeds obtained from seeds not showing evidence of fungal colonization. When supplied with Se, the Alternaria-colonized seedlings had lower shoot Se and sulfur levels than seedlings from uncolonized seeds. In conclusion, A. tenuissima may contribute to the Se0 observed earlier in A. bisulcatus, and affect host growth and Se accumulation. A2 is sensitive to the Se levels found in its host’s tissues, but may avoid Se toxicity by occupying low-Se areas (seed coat, apoplast) and converting plant Se to non-toxic Se0. These findings illustrate the potential for hyperaccumulator endophytes to affect plant properties relevant for phytoremediation. Facultative endophytes may also be applicable in bioremediation and biofortification, owing to their capacity to turn toxic inorganic forms of Se into non-toxic or even beneficial, organic forms with anticarcinogenic properties.},
doi = {10.3389/fpls.2018.01213},
journal = {Frontiers in Plant Science},
number = ,
volume = 9,
place = {United States},
year = {2018},
month = {8}
}

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Works referenced in this record:

Spatial Imaging, Speciation, and Quantification of Selenium in the Hyperaccumulator Plants Astragalus bisulcatus and Stanleya pinnata
journal, August 2006

  • Freeman, John L.; Zhang, Li Hong; Marcus, Matthew A.
  • Plant Physiology, Vol. 142, Issue 1
  • DOI: 10.1104/pp.106.081158

Interactions of fungip with toxic metals
journal, May 1993


Selenium Hyperaccumulators Facilitate Selenium-Tolerant Neighbors via Phytoenrichment and Reduced Herbivory
journal, September 2011

  • El Mehdawi, Ali F.; Quinn, Colin F.; Pilon-Smits, Elizabeth A. H.
  • Current Biology, Vol. 21, Issue 17
  • DOI: 10.1016/j.cub.2011.07.033

Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related nonaccumulators
journal, November 2006


Selenium Distribution and Speciation in the Hyperaccumulator Astragalus bisulcatus and Associated Ecological Partners
journal, May 2012

  • Valdez Barillas, José R.; Quinn, Colin F.; Freeman, John L.
  • Plant Physiology, Vol. 159, Issue 4
  • DOI: 10.1104/pp.112.199307

Characterization of rhizosphere fungi from selenium hyperaccumulator and nonhyperaccumulator plants along the eastern Rocky Mountain Front Range
journal, July 2011

  • Wangeline, Ami L.; Valdez, J. Rodolfo; Lindblom, Stormy Dawn
  • American Journal of Botany, Vol. 98, Issue 7
  • DOI: 10.3732/ajb.1000369

Dissimilatory Metal Reduction
journal, October 1993


Reduction of selenium oxyanions by unicellular, polymorphic and filamentous fungi: Cellular location of reduced selenium and implications for tolerance
journal, March 1995

  • Gharieb, M. M.; Wilkinson, S. C.; Gadd, G. M.
  • Journal of Industrial Microbiology, Vol. 14, Issue 3-4
  • DOI: 10.1007/BF01569943

Beamline 10.3.2 at ALS: a hard X-ray microprobe for environmental and materials sciences
journal, April 2004

  • Marcus, Matthew A.; MacDowell, Alastair A.; Celestre, Richard
  • Journal of Synchrotron Radiation, Vol. 11, Issue 3
  • DOI: 10.1107/S0909049504005837

Selenium Accumulation in Plants—Phytotechnological Applications and Ecological Implications
journal, January 2011

  • Barillas, José Rodolfo Valdez; Quinn, Colin F.; Pilon-Smits, Elizabeth A. H.
  • International Journal of Phytoremediation, Vol. 13, Issue sup1
  • DOI: 10.1080/15226514.2011.568542

Biogeochemistry of selenium and its impact on food chain quality and human health
journal, June 2005


Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection
journal, August 2003


Seleno amino compounds from Astragalus bisulcatus isolation and identification of γ-L-glutamyl-Se-methyl-seleno-L-cysteine and Se-methylseleno-L-cysteine
journal, November 1969

  • Nigam, S. N.; McConnell, W. B.
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 192, Issue 2
  • DOI: 10.1016/0304-4165(69)90354-7

S ELENIUM IN H IGHER P LANTS
journal, June 2000

  • Terry, N.; Zayed, A. M.; de Souza, M. P.
  • Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 51, Issue 1
  • DOI: 10.1146/annurev.arplant.51.1.401

Toxicology of selenium: A review
journal, January 1980


An expanded multilocus phylogeny does not resolve morphological species within the small-spored Alternaria species complex
journal, January 2009

  • Andrew, M.; Peever, T. L.; Pryor, B. M.
  • Mycologia, Vol. 101, Issue 1
  • DOI: 10.3852/08-135

The fascinating facets of plant selenium accumulation – biochemistry, physiology, evolution and ecology
journal, November 2016

  • Schiavon, Michela; Pilon‐Smits, Elizabeth A. H.
  • New Phytologist, Vol. 213, Issue 4
  • DOI: 10.1111/nph.14378

Effects of selenium hyperaccumulation on plant-plant interactions: evidence for elemental allelopathy?
journal, March 2011


Nitric acid digestion and multi‐element analysis of plant material by inductively coupled plasma spectrometry
journal, January 1987

  • Zarcinas, B. A.; Cartwright, B.; Spouncer, L. R.
  • Communications in Soil Science and Plant Analysis, Vol. 18, Issue 1
  • DOI: 10.1080/00103628709367806

A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures
journal, July 1962


Comparative Genomics of Trace Elements: Emerging Dynamic View of Trace Element Utilization and Function
journal, October 2009

  • Zhang, Yan; Gladyshev, Vadim N.
  • Chemical Reviews, Vol. 109, Issue 10
  • DOI: 10.1021/cr800557s

Quantitative Elemental Analyses by Plasma Emission Spectroscopy
journal, October 1978


Influence of microbial associations on selenium localization and speciation in roots of Astragalus and Stanleya hyperaccumulators
journal, April 2013


Roles of rhizobial symbionts in selenium hyperaccumulation in Astragalus (Fabaceae)
journal, November 2014

  • Alford, Élan R.; Lindblom, Stormy D.; Pittarello, Marco
  • American Journal of Botany, Vol. 101, Issue 11
  • DOI: 10.3732/ajb.1400223

Selenium accumulation in flowers and its effects on pollination
journal, July 2011


Selenium Biofortification and Phytoremediation Phytotechnologies: A Review
journal, January 2017

  • Schiavon, Michela; Pilon-Smits, Elizabeth A. H.
  • Journal of Environment Quality, Vol. 46, Issue 1
  • DOI: 10.2134/jeq2016.09.0342

Nucleic Acid–Based Pathogen Detection in Applied Plant Pathology
journal, May 2008


Selenium-Tolerant Diamondback Moth Disarms Hyperaccumulator Plant Defense
journal, November 2006


Ecological aspects of plant selenium hyperaccumulation: Ecology of selenium hyperaccumulation
journal, December 2011


Selenium Biochemistry
journal, June 1990


Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata
journal, May 2010

  • Freeman, John L.; Tamaoki, Masanori; Stushnoff, Cecil
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.156570

Metallophytes—a view from the rhizosphere
journal, July 2010

  • Alford, Élan R.; Pilon-Smits, Elizabeth A. H.; Paschke, Mark W.
  • Plant and Soil, Vol. 337, Issue 1-2
  • DOI: 10.1007/s11104-010-0482-3

Brassica juncea can improve selenite and selenate abatement in selenium contaminated soils through the aid of its rhizospheric bacterial population
journal, May 2006


Selenium hyperaccumulators harbor a diverse endophytic bacterial community characterized by high selenium resistance and plant growth promoting properties
journal, March 2015

  • Sura-de Jong, Martina; Reynolds, Ray J. B.; Richterova, Klara
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00113

Enhanced decomposition of selenium hyperaccumulator litter in a seleniferous habitat—evidence for specialist decomposers?
journal, June 2010


Rhizosphere Bacteria Enhance Selenium Accumulation and Volatilization by Indian Mustard
journal, February 1999

  • de Souza, Mark P.; Chu, Dara; Zhao, May
  • Plant Physiology, Vol. 119, Issue 2
  • DOI: 10.1104/pp.119.2.565

X-ray absorption spectroscopy of selenium-containing amino acids
journal, December 1999

  • Pickering, I. J.; George, Graham N.; Van Fleet-Stalder, Verena
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 4, Issue 6
  • DOI: 10.1007/s007750050352