Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree

Luis C. Mejía, Edward A. Herre, Jed P. Sparks, Klaus Winter, Milton N. García, Sunshine A. Van Bael, Joseph Stitt, Zi Shi, Yufan Zhang, Mark J. Guiltinan, Siela N. Maximova

Research output: Contribution to journalArticle

46 Citations (Scopus)

Abstract

It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.

Original languageEnglish (US)
Article number479
JournalFrontiers in Microbiology
Volume5
Issue numberSEP
DOIs
StatePublished - Jan 1 2014

Fingerprint

Endophytes
Fungi
Cacao
Photosynthesis
Nitrogen
Heterotrophic Processes
Carbon Isotopes
Colletotrichum
Genes
Anthozoa
Herbivory
Symbiosis
Lignin
Cellulose
Cost-Benefit Analysis
Insects
Vertebrates
Up-Regulation
Costs and Cost Analysis
Research

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Microbiology (medical)

Cite this

Mejía, Luis C. ; Herre, Edward A. ; Sparks, Jed P. ; Winter, Klaus ; García, Milton N. ; Van Bael, Sunshine A. ; Stitt, Joseph ; Shi, Zi ; Zhang, Yufan ; Guiltinan, Mark J. ; Maximova, Siela N. / Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. In: Frontiers in Microbiology. 2014 ; Vol. 5, No. SEP.
@article{56994e86332a429daf45a57a9279cd96,
title = "Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree",
abstract = "It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.",
author = "Mej{\'i}a, {Luis C.} and Herre, {Edward A.} and Sparks, {Jed P.} and Klaus Winter and Garc{\'i}a, {Milton N.} and {Van Bael}, {Sunshine A.} and Joseph Stitt and Zi Shi and Yufan Zhang and Guiltinan, {Mark J.} and Maximova, {Siela N.}",
year = "2014",
month = "1",
day = "1",
doi = "10.3389/fmicb.2014.00479",
language = "English (US)",
volume = "5",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S. A.",
number = "SEP",

}

Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. / Mejía, Luis C.; Herre, Edward A.; Sparks, Jed P.; Winter, Klaus; García, Milton N.; Van Bael, Sunshine A.; Stitt, Joseph; Shi, Zi; Zhang, Yufan; Guiltinan, Mark J.; Maximova, Siela N.

In: Frontiers in Microbiology, Vol. 5, No. SEP, 479, 01.01.2014.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree

AU - Mejía, Luis C.

AU - Herre, Edward A.

AU - Sparks, Jed P.

AU - Winter, Klaus

AU - García, Milton N.

AU - Van Bael, Sunshine A.

AU - Stitt, Joseph

AU - Shi, Zi

AU - Zhang, Yufan

AU - Guiltinan, Mark J.

AU - Maximova, Siela N.

PY - 2014/1/1

Y1 - 2014/1/1

N2 - It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.

AB - It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E-) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.

UR - http://www.scopus.com/inward/record.url?scp=84907997853&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84907997853&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2014.00479

DO - 10.3389/fmicb.2014.00479

M3 - Article

C2 - 25309519

AN - SCOPUS:84907997853

VL - 5

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

IS - SEP

M1 - 479

ER -