6 NLR Function in Fungi as Revealed by the Study of Self/Non-self
Recognition Systems
ASEN DASKALOV
1,2 , WITOLD DYRKA
3
, SVEN J. SAUPE
4
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
II. NLRs in Fungal Incompatibility . . . . . . . . . . . . 124
III. In Silico Survey of Fungal NLR
Repertoires . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
IV. Evolution and Variability of NLR Repertoires
in Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130
V. Prion-Forming Domains in NLR
Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132
VI. Evolutionary Origin of NLRs: Parallel Versus
Convergent Evolution . . . . . . . . . . . . . . . . . . . . . . . 134
VII. The Exaptation Model: How to Craft an
Allorecognition System . . . . . . . . . . . . . . . . . . . . . 136
VIII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
I. Introduction
All organisms rely on innate immunity to cope
appropriately with challenges imposed by a
variety of biotic interactions. In particular
both plants and animals employ different
types of germ-line-encoded pattern recognition
receptors (PRR) to mount a scaled response to
various forms of microbial infection. In addition, some of these receptors also appear to play
a role in establishing beneficial relationships
making it increasingly clear that biotic interactions align along a continuum ranging from
pathogenicity to symbiosis (Lipinski and
Rosenstiel 2013; Sellge and Kufer 2015).
Among these PRRs, the cytoplasmic NLR
receptors represent a large and highly diversified family (NLR for Nod-like receptors or NBSLRR, nucleotide binding site and leucine-rich
repeats) (Duxbury et al. 2016; Jones et al. 2016;
Meunier and Broz 2017; Zhang et al. 2017).
Plant and animal NLRs share a similar domain
architecture and function. This similarity in
domain organization is currently proposed to
result from convergent evolution in plants and
animals (Urbach and Ausubel 2017). These
intracellular receptors have a typical tripartite
domain architecture with a central nucleotidebinding and oligomerization domain (NOD)
(Leipe et al. 2004) (most often of the NB-ARC
type in plants and NACHT type in animals)
flanked C-terminally by a LRR domain and Nterminally by an effector or signaling domain,
thought to be responsible for mediating the
downstream host responses including programmed cell death. In plant systems, one distinguishes PAMP-triggered immunity (PTI)
where the immune response relies on the detection of pathogen-associated molecular patterns
(PAMPs), from effector-triggered immunity
(ETI), where the cell response is dependent on
detection of modifications of the host state by
pathogen-secreted effectors (Jones and Dangl
2006; Jones et al. 2016). The “guard model”
was proposed as a frame for this form of
immune response. The receptors (“guards”)
monitor the integrity of host proteins (“guardees”) which are the target of pathogen effectors that either degrade or modify these targets
as part of their host invasion scheme. As further
1 The Plant and Microbial Biology Department, University of
California, California, USA
2 Institut Europe ´en de Chimie et Biologie (IECB), Pessac,
France
3 Politechnika Wrocławska, Wydział Podstawowych Problemo ´w Techniki, Katedra Inz ˙ynierii Biomedycznej, Wrocław,
Poland
4 Non-self Recognition in Fungi, UMR5095 Institut de Biochimie et Ge ´ne ´tique Cellulaires, CNRS – Universite ´ de Bordeaux,
Bordeaux Cedex, France; e-mail: sven.saupe@ibgc.cnrs.fr
Genetics and Biotechnology, 3 rd Edition
The Mycota II
J.P. Benz, K. Schipper (Eds.)
© Springer Nature Switzerland AG 2020
Recognition Systems
ASEN DASKALOV
1,2 , WITOLD DYRKA
3
, SVEN J. SAUPE
4
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
II. NLRs in Fungal Incompatibility . . . . . . . . . . . . 124
III. In Silico Survey of Fungal NLR
Repertoires . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
IV. Evolution and Variability of NLR Repertoires
in Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130
V. Prion-Forming Domains in NLR
Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132
VI. Evolutionary Origin of NLRs: Parallel Versus
Convergent Evolution . . . . . . . . . . . . . . . . . . . . . . . 134
VII. The Exaptation Model: How to Craft an
Allorecognition System . . . . . . . . . . . . . . . . . . . . . 136
VIII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
I. Introduction
All organisms rely on innate immunity to cope
appropriately with challenges imposed by a
variety of biotic interactions. In particular
both plants and animals employ different
types of germ-line-encoded pattern recognition
receptors (PRR) to mount a scaled response to
various forms of microbial infection. In addition, some of these receptors also appear to play
a role in establishing beneficial relationships
making it increasingly clear that biotic interactions align along a continuum ranging from
pathogenicity to symbiosis (Lipinski and
Rosenstiel 2013; Sellge and Kufer 2015).
Among these PRRs, the cytoplasmic NLR
receptors represent a large and highly diversified family (NLR for Nod-like receptors or NBSLRR, nucleotide binding site and leucine-rich
repeats) (Duxbury et al. 2016; Jones et al. 2016;
Meunier and Broz 2017; Zhang et al. 2017).
Plant and animal NLRs share a similar domain
architecture and function. This similarity in
domain organization is currently proposed to
result from convergent evolution in plants and
animals (Urbach and Ausubel 2017). These
intracellular receptors have a typical tripartite
domain architecture with a central nucleotidebinding and oligomerization domain (NOD)
(Leipe et al. 2004) (most often of the NB-ARC
type in plants and NACHT type in animals)
flanked C-terminally by a LRR domain and Nterminally by an effector or signaling domain,
thought to be responsible for mediating the
downstream host responses including programmed cell death. In plant systems, one distinguishes PAMP-triggered immunity (PTI)
where the immune response relies on the detection of pathogen-associated molecular patterns
(PAMPs), from effector-triggered immunity
(ETI), where the cell response is dependent on
detection of modifications of the host state by
pathogen-secreted effectors (Jones and Dangl
2006; Jones et al. 2016). The “guard model”
was proposed as a frame for this form of
immune response. The receptors (“guards”)
monitor the integrity of host proteins (“guardees”) which are the target of pathogen effectors that either degrade or modify these targets
as part of their host invasion scheme. As further
1 The Plant and Microbial Biology Department, University of
California, California, USA
2 Institut Europe ´en de Chimie et Biologie (IECB), Pessac,
France
3 Politechnika Wrocławska, Wydział Podstawowych Problemo ´w Techniki, Katedra Inz ˙ynierii Biomedycznej, Wrocław,
Poland
4 Non-self Recognition in Fungi, UMR5095 Institut de Biochimie et Ge ´ne ´tique Cellulaires, CNRS – Universite ´ de Bordeaux,
Bordeaux Cedex, France; e-mail: sven.saupe@ibgc.cnrs.fr
Genetics and Biotechnology, 3 rd Edition
The Mycota II
J.P. Benz, K. Schipper (Eds.)
© Springer Nature Switzerland AG 2020