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Editorial overview: Biotic interactions: The diverse

and dynamic nature of perception and response
in plant interactions: from cells to communities
Uta Paszkowski and D Barry Scott
Current Opinion in Plant Biology 2015, 26:v–viii

For a complete overview see the Issue

Available online 17th August 2015

http://dx.doi.org/10.1016/j.pbi.2015.08.001

1369-5266/Crown Copyright # 2015 Published by

Elsevier Ltd. All rights reserved.

Uta Paszkowski
Department of Plant Sciences, Cambridge
University, Downing Street, Cambridge CB2
3EA, United Kingdom
e-mail: up220@cam.ac.uk
Uta Paszkowski is a Lecturer in the
Department of Plant Sciences at Cambridge
University. Her research aims at the elucidation
of molecular mechanisms underlying the
development of the AM symbioses and the
benefit it confers to cereal phosphate nutrition.
Her team established rice and maize as
monocotyledonous models for the study of
molecular genetics of AM symbioses, and
settled functional conservation of certain
symbiosis signaling components between
dicotyledon and monocotyledons. She
introduced the full complement of phosphate
transporters of a crop plant, identified the first
AM specific transporter PT11, and resolved
symbiotic phosphate acquisition in rice.
D Barry Scott
Institute of Fundamental Sciences, Massey
University, Private Bag 11 222, Palmerston
North 4442, New Zealand
e-mail: d.b.scott@massey.ac.nz
Barry Scott FRSNZ is Professor of Molecular
Genetics at Massey University and a Principal
Investigator in the Bioprotection Research
Centre, a national center of research
excellence. His research focuses on under-
standing the biology of mutualistic symbiotic
interactions between Epichloë festucae and
temperate grass species. His group was
responsible for identifying and characterizing
endophyte genes responsible for the synthesis
of some of the bioprotective metabolites
unique to this symbiosis. His team also
identified a number of key endophyte signaling
genes required for hyphal cell–cell fusion and
stable maintenance of the aerial hyphal
network that characterizes this symbiosis.
Plants naturally interact with a broad range of taxonomically diverse organ-
isms, such as other plants, mammals, insects, and diverse microbes. These
interactions have important consequences for plant development, growth
and survival. They influence community structure and dynamics and may
also affect plant evolution. In this series of commissioned reviews we
intended to capture the diversity of these interactions and the cellular,
developmental, evolutionary and ecological outcomes. The application of
advanced technologies, foremost next generation sequencing, has dramati-
cally improved our understanding of the molecular basis of plant interactions
and the evolution of the organisms comprising these associations.
Molecular evolution
The interactive life-style of plants and their invaders is mirrored in the
specificities of their genetic ‘equipment’. The steadily increasing genome
information shapes our understanding of both the evolutionary relationship
of species and the evolution of gene function and complexity.
Secondary metabolites are central to defining the ecological niche and
environmental functioning of fungi. Joseph Spatofora and Kathryn
Bushley describe how fungal phylogenomics of secondary metabolite bio-
synthesis gene clusters has revealed a more extensive genome-encoded
capacity for metabolic diversity and complexity than previously assumed.
The authors provide mechanistic explanations for the often surprisingly
incongruent evolutionary history of metabolic gene clusters across a broader
range of fungal taxa, focusing on plant-infecting members of the Ascomycota
and non-ribosomal peptide synthetases (NRPS) as examples.
In contrast, genetic diversity in the ancient asexual, beneficial arbuscular
mycorhizal (AM) fungi has long been suggested to be achieved by geneti-
cally non-identical nuclei contained within the hyphal syncytium; however,
the first genome sequences show otherwise. Peter Young updates us on this
controversy and evaluates the pros and cons for heterokaryosis in the light of
hundreds of millions of years of need for adaptation in the absence of sex. He
posits that the resemblance to mitochondrial inheritance in ‘standard’
organisms may provide guidance for the creation and persistence of genetic
diversity.
The mutualistic root association with nitrogen-fixing bacteria is a highly
desirable trait to be introduced into major (cereal) crops but is naturally

www.sciencedirect.com Current Opinion in Plant Biology 2015, 26:v–viii

vi Biotic interactions
restricted to the family of the Fabaceae and a few other
plant species. Pierre-Marc Delaux et al. emphasize com-
parative phylogenetics and phylogenomics as a diagnostic
tool for genome specificities associated with nodulation,
and also to systematically dissect the evolutionary transi-
tion towards nodulation and the mechanistic under-
pinnings. A comprehensive molecular understanding
combined with high-throughput synthetic biology tools
may ultimately permit the reconstruction of the evolu-
tionary path and enable the engineering of bacterial
nitrogen fixation into grain crops.
Horizontal gene transfer (HGT) in plants receives in-
creasing scientific attention due to its potential impact on
genome evolution. Charles Davis and Zhenxiang Xi
highlight the particularly high frequency of HGT in
parasitic plants, which predominantly involves mitochon-
drial DNA. The intimacy of the interaction of parasitic
plants with their hosts in conjunction with mitochondrial
properties for DNA uptake and integration may mecha-
nistically explain the high rate of transgene transfer
specifically to mitochondrial genomes. However nuclear
HGT and host-transgene transcription from the parasite
also occurs, thereby possibly contributing to the ‘evolu-
tion of novelty’ of parasitic plant genomes. Intriguingly,
an ‘accumulation’ of transgenes in the genomes of para-
sitic plants reflects the history of associations and invites
the study of HGT and the origin of parasitism in plants.
Communication
The identification of short and long distance signals, how
they are perceived and transmitted, is important in un-
derstanding the resulting cellular outcomes and ultimate-
ly how organisms interact in the field.
While much is known about chemotropic interactions of
bacteria with bacteria, and plants with bacteria, relatively
little is known about how plants communicate with fungi.
The review by David Turrà and Antonio Di Pietro
highlights how studies in the root pathogen, Fusarium
oxysporum, identify new signals and pathways for chemot-
ropism that were hitherto not known from studies in the
model organisms Saccharomyces cerevisiae and Neurospora
crassa. Their review also provides a good overview of
chemotropism in mating in S. cerevisiae and highlights
new signaling components required for cell–cell self
fusion in N. crassa.
Lauren Ryder and Nicholas Talbot provide an overview
of how foliar pathogenic fungi breach the cuticle of their
plant hosts through formation of appressoria. Control of
the cell cycle has been shown to be crucial for appresso-
rium development in both Magnaporthe oryzae and Ustilago
maydis and is likely to be a conserved process. Remodel-
ing of the actin cytoskeleton, mediated by septin
GTPases, is a key step in the differentiation of this
swollen infection structure and requires the sequential
Current Opinion in Plant Biology 2015, 26:v–viii
action of two NADPH oxidase complexes. Interestingly,
melanin is not necessary for maintenance of turgor pres-
sure in the appressoria of several pathogens. Recent work
shows that penetration pegs in some phytopathogenic
fungi are foci for delivery of effectors into the host.
Besides small peptides and metabolites, macromolecules
such as RNA have now been shown to be key signals for
communication between closely associated organisms.
The review by Gungjune Kim and James Westwood
highlights the power of massive parallel sequencing in
providing insights into macromolecular trafficking in a
parasitic plant — plant host interaction. They show that
mRNAs are exchanged between Cuscata, a plant parasite,
and its host plants in a bidirectional fashion. While there
is still no direct evidence for a developmental outcome
resulting from exchange of mRNA they do show that
engineering an RNA silencing signal into the host results
in gene silencing in the parasite.
Important to the outcome of any plant host interaction is
the modulation of the host innate immunity response.
Tomonori Shinya et al. provide an overview of the role
LysM receptor complexes play in perception of chitin
fragments from the cell wall of pathogenic fungi and how
in turn fungi suppress this response through secretion of
specific effectors. They highlight how chitin-related
molecules also serve as signals for the establishment of
Rhizobium and arbuscular mycorrhizal symbiotic associa-
tions and how the rice receptor kinase has a dual role in
responding to these symbiosis signals and inducing chi-
tin-mediated immunity. This discovery highlights the
close evolutionary relationship in the plant response to
defense and symbiotic signals.
Enrico Gobbato reviews our current understanding of
how arbuscular mycorrhiza fungi and rhizobia bacteria
establish root endosymbiosis and the considerable prog-
ress that has been made in understanding the components
upstream and downstream of the common symbiosis
signaling pathway, how they are connected, and what
outstanding questions remain in defining signaling spec-
ificity in these two associations. As in the preceding
review he highlights the reciprocal connection between
defense and symbiosis signaling through genetic analysis
of the LysM receptor like kinases from Lotus japonicus and
Medicago truncatula. Molecular evolution studies indicate
that ancestral receptor-like kinases had a function in
symbiosis rather than defense-related chitin receptors.
Epigenetics
It is now well established that post-transcriptional regu-
lation processes such as gene silencing by small RNAs
and chromatin modification are very important regulatory
layers in determining both temporal and spatial expres-
sion of genes. In addition, some small RNAs are mobile
signals that transmit gene silencing from cell to cell and
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from one organism to another. These results have impor-
tant implications in understanding inter-organism com-
munication and how that controls both development and
pathogenicity.
While the mechanisms that underlie viral induced gene
silencing (VIGS) in plants are well characterized much
less is known about host induced gene silencing (HIGS)
or filamentous organism-induced gene silencing (FIGS).
In a very helpful review as to how this gap might be
bridged David Baulcombe provides an overview of RNA
silencing in virus defense and how this knowledge may
provide a conceptual and mechanistic framework for
RNA silencing in general, highlighting a number of
defined features that are important for VIGS of possible
relevance for understanding the other interactions He
proposes key experiments that still need to be done to
better understand the silencing mechanisms operating
between filamentous organisms and plants.
A key component to the multi-layered plant immune
system is the counter–counter defense response triggered
by host perception of the pathogen through NOD-like
receptors (NLRs) or nucleotide-binding leucine-rich re-
peat receptors (NB-LRRs). In their review Thierry
Halter and Lionel Navarro focus on post-transcriptional
regulatory processes including control of abundance and
composition of NLR transcripts through nonsense medi-
ated decay and alternative splicing processes. They em-
phasize the importance of a dynamic regulatory system
for controlling NLR transcripts to achieve a rapid plant
defense response while limiting the fitness cost triggered
by the plant immune response. A key take home message
from this review is the evolutionary convergence between
small RNA biogenesis and splicing in plants.
A very exciting area of new research is the role of small
RNAs in mediating plant immune response and pathogen
virulence. The review by Arne Weiberg and Hailing Jin
summarizes the latest findings on what is known about
the movement of small RNAs between interacting organ-
isms and the mechanisms responsible for cross-kingdom
RNA interference. They draw on an extensive volume of
literature of known processes in microbes, plants and
animals to provide an overview of the similarities and
differences between endogenous sRNA-mediated regu-
lation within an organism and sRNA-mediated cross
kingdom RNAi between host and pathogen. The authors
also suggest potential strategies that could be developed
based on this knowledge to generate pest- and pathogen-
resistant crops.
The review by Jessica Soyer et al. highlights the impor-
tance of chromatin-based control of gene expression,
relevant to successful infection in plant-associated fungi.
Whole genome sequencing of plant associated fungi and
oomycetes has revealed that the landscape of the genome
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Editorial overview Paszkowski and Scott vii
is highly variable and that many of the genes important for
symbiotic interactions are embedded within regions of
the genome that are rich in transposon elements. In
axenic culture these regions of the genome are highly
heterochromatic but once the fungi interact with their
host the chromatin is remodeled to allow for high-level
gene expression at a particular stage of development.
Effectors
Plant-infecting organisms employ small-secreted effector
molecules to modulate the host physiology in their favor.
This strategy is not only common across pathogenic
bacteria, fungi and oomycetes, but extends to mutualistic
microbes, and also to worms and insects. What is more,
plants use effector peptides that act upon the invading
organism.
Concentrating on mycorrhizal symbioses Jonathan Plett
and Francis Martin summarize how effector proteins of
these beneficial fungi remodel plant signaling. The
authors draw particular attention to the fact that the same
plant hormonal signaling pathways are targeted by effec-
tors from both beneficial and pathogenic fungi. Remark-
ably, ‘beneficial effectors’ can drive re-programming of
the host jasmonic acid signaling towards favoring mutu-
alism over defense. Therefore, the regulation of plant
hormonal activities is hypothesized to play a decisive role
for the outcome of the plant–microbe interactions.
Similarly, effector molecules also modulate plant defense
hormone signaling during herbivory and re-direct host
responses to benefit the attacking insect. Flor Acevedo
et al. untangle this hugely complex signaling scenario which
in addition to diverse effectors is composed of multiple
types of ‘molecular patterns’, originating from wounded
plant tissue (DAMPs), insect fluids (HAMPs) and from
insect-associated microbes (MAMPs). They highlight stra-
tegic similarities across otherwise context-specific signaling
and emphasize the pressing need for comprehensive
‘omics’-based proteome and metabolome diagnostics, in
particular of HAMPS and effectors, combined with the
molecular elucidation of herbivore perception.
Remarkably, plants also encode effectors, eventually tip-
ping the scale between defense and mutualistic associa-
tions. Amongst the group of short cysteine-rich effector
peptides, anti-microbial defensins are involved in innate
immunity, whereas the highly abundant defensin-like
nodule-specific cysteine-rich peptides (NCR) function
in mutualism of some legumes with nitrogen-fixing bacte-
ria. The review by Gergely Maróti et al. explains the role
individual symbiotic NCRs play in governing the terminal
differentiation of bacteria to nitrogen-fixing bacteroids and
in limiting bacterial proliferation. They analyze the phy-
logenetic relationship of the effector peptides, concentrat-
ing on Medicago truncatula, and discuss why NRCs may
Current Opinion in Plant Biology 2015, 26:v–viii
viii Biotic interactions
have diversified in some leguminous plant species but are
absent from others.
Metabolism
Understanding how the metabolism of the plant is mod-
ulated in response to microbial infection or colonization is
crucial for gaining insights into the molecular mecha-
nisms that underlie plant–microbe interactions.
The review by Ivo Feussner and Andrea Polle takes a
systems-biology approach concentrating on how knowl-
edge gained from the proteome and metabolome contrib-
utes to a fuller understanding of plant–microbe
interactions. A good example of the spatial resolution
afforded by proteomics is the identification of specific
components of basal immunity in the apoplast of the plant
and identification of proteins with no obvious signal
sequence for secretion. Analysis of the metabolome has
led to the discovery of small molecules important for
plant–microbe interactions such as those involved in
systemic acquired resistance. They also provide an over-
view of the technologies themselves, and the develop-
ment of tools to analyze the large and complex data sets
generated in proteomic and metabolomic workflows.
The importance of microalgae and cyanobacteria in total
global carbon fixation, and in many cases their obligate
requirement for exogenous supplies of certain nutrients
with relevance in evolutionary adaptation, is highlighted
in the review by Matthew Cooper and Alison Smith. As
with terrestrial symbioses, interkingdom signaling is im-
portant in the establishment and maintenance of these
globally important interactions. Algae can sense specific
signals produced by bacterial biofilms to identify suitable
habitats for growth and in some cases produce metabolite
mimics that disrupt bacterial signaling reducing the inci-
dence of infections. The biotechnological potential of this
group of organisms for the production of high value
products and biofuel molecules is also highlighted.
The review by Rabea Schweiger and Caroline Müller
summarizes the effect of arbuscular mycorrhizal infection
of the roots and how that leads to changes in the metabolite
composition of the leaf and in some cases on phytoprotec-
tion against different abiotic and biotic stresses. They also
point out the pitfalls in measuring metabolite changes in
the leaves due to experimentally easily introduced varia-
tion and recommend strategies that enable monitoring the
desired parameters with improved precision.
The penalties of a hyper-active immune system on plant
fitness have been repeatedly documented. Focusing on
root development, Ruth Eichmann and Patrick Schäfer
Current Opinion in Plant Biology 2015, 26:v–viii
analyze the inhibitory growth-immunity cross talk on the
molecular level. Instead of attributing it to a nutritional
effect they propose a hormonal signaling link that via the
activity of transcription factors negatively regulates
plant growth. As a plausible explanation they introduce
a concept whereby the disturbance or re-direction of
hormone activities interferes with the cell-cycle machin-
ery, ultimately resulting in the suppression of meristem
activity.
Communities
The relationship between individual plants and corre-
sponding interacting organism(s) to a large extent is
defined by the species composition and dynamics of
the natural- or agro-ecosystem environment.
The importance of the interplay between the microbiome
and plant roots, and their reciprocal modulation, is
highlighted by Sarah Sloan and Sarah Lebeis. ‘Metabolic
complementation’ and/or host ‘priming’ as driving forces
in shaping the composition of inter-organismic commu-
nities are discussed amongst other emerging mechanisms.
In addition, microbial interactions occur and impact on
plant performance, the latter being furthermore influ-
enced by neighboring plants. The need for an increased
level of accuracy by which the effects of host plants on the
microbiome and vice versa are defined is emphasized, and
concomitantly the importance of applying the steadily
advancing technologies.
Concentrating on common mycorrhizal networks as a
belowground plant-to-plant herbivore warning pipelines,
Lucy Gilbert and David Johnson review the role of these
networks in the herbivore–plant–mycorrhiza continuum.
They examine the potential cost consequences of this
sophisticated ‘social’ signaling for the plant and propose a
possible link between the plants’ carbon management
and the yet elusive metabolite signal. Given the ability of
mycorrhizal fungi to simultaneously colonize different
plant species and transmit informative signals between
them, the impact on community dynamics is to be con-
sidered.
Flower pollination by animals is an integral part to many
global crop production systems. Emily Bailes et al. not
only highlight the important contribution of these inter-
actions for food security but also flag the growing threats
such as the diminishing natural and managed pollinator
populations. The authors define the existing potential
and floral traits suitable as targets for breeding and
biotechnology based strategies and therefore spur the
intensification of plant-pollinator research, aiming at
insect-friendly higher yielding crops.
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