Characterization of mRNA populations associated with the translational machinery (translatome) is shedding light on the molecular mechanisms of plant environmental responses. The work presented by Meteignier et al. (2017) describes how selective changes in translation modulate the transition from growth to defense responses in Arabidopsis, revealing new similarities between plant and animal immunity.Facultad de Ciencias Exacta

Blanco, Flavio Antonio

Zanetti, María Eugenia

Journal of Experimental Botany

English

SEDICI - Repositorio de la UNLP

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Insight
Translational switching from growth to defense – a common 
role for TOR in plant and mammalian immunity?
María Eugenia Zanetti1,* and Flavio A. Blanco1
1 Instituto de Biotecnología y Biología Molecular, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, CCT-La Plata, 
CONICET, La Plata, Argentina
* Correspondence: ezanetti@biol.unlp.edu.ar
Characterization of mRNA populations associ-
ated with the translational machinery (translatome) 
is shedding light on the molecular mechanisms of 
plant environmental responses. The work presented 
by Meteignier et  al. (2017) describes how selec-
tive changes in translation modulate the transition 
from growth to defense responses in Arabidopsis, 
revealing new similarities between plant and animal 
immunity.
Plants have developed sophisticated mechanisms to adjust 
their developmental programs in response to changes in 
their environment. This adaptation largely depends on selec-
tive changes in gene expression, which include transcrip-
tional and post-transcriptional control. Transcriptional 
changes provide a long-term response and, usually, are 
triggered by a signaling pathway initiated by signal percep-
tion that culminates in the activation of  transcription fac-
tors in the nucleus. Transcriptome (the population of  total 
cellular mRNAs) studies have enabled the identification of 
genes that are crucial for adaptation in numerous plant spe-
cies. However, mRNA abundance and protein levels do not 
always correlate due to co- and post-transcriptional mecha-
nisms controlling gene expression. Among such post-tran-
scriptional mechanisms, mRNA translation plays a crucial 
role in controlling the amount of  protein present in a cell or 
tissue. Translational control has been observed in a number 
of  developmental processes in plants, as well as in response 
to environmental cues.
During the past decade, an increasing number of studies 
have focused on changes in the translatome (the population 
of actively translating mRNAs) during phase-transitions or 
perturbation caused by endogenous or exogenous signals. 
From these studies we know that translational control can 
be global, affecting most cellular mRNAs, or selective, affect-
ing just a subset. Global translational repression has been 
observed during stresses that produce a cellular ‘energy cri-
sis’, such as hypoxia (Branco-Price et al., 2005; Branco-Price 
et al., 2008; Mustroph et al., 2009), heat (Yanguez et al., 2013), 
and drought (Kawaguchi and Bailey-Serres, 2002; Kawaguchi 
et  al., 2004; Lei et  al., 2015). On the other hand, selective 
translational regulation has been associated with dark/light 
transitions (Juntawong and Bailey-Serres, 2012), photomor-
phogenesis (Liu et al., 2013), daily clock cycles (Missra et al., 
2015), and symbiosis with nitrogen-fixing bacteria (Reynoso 
et al., 2013).
Meteignier et  al. (2017) show that selective translational 
control also occurs during plant immunity. A  remarkable 
characteristic of translational regulation is that it enables 
rapid adjustment of the proteome using the existing tran-
scriptome, thus providing cells or tissues with a fast and flex-
ible response for adapting to changes in their environment, as 
in the case of the hypersensitive response triggered by some 
plant pathogens. This rapid response is frequently achieved by 
controlling the initiation step of translation, i.e. by increasing 
or decreasing the number of molecules of individual tran-
scripts that are recruited to the translational machinery with-
out a change in transcript abundance or even, in some cases, 
with an opposite change in transcript abundance.
© The Author 2017. Published by Oxford University Press on behalf of the Society for Experimental Biology.  
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), 
which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
2078 |
Translational control of immunity in plants 
and animals
Plant immunity against pathogens relies on mechanisms that 
allow host cells to perceive pathogens and mount a rapid 
and effective response that limits their spread. The work of 
Meteignier et al. (2017) used TRAP-seq technology (Box 1) 
to characterize the rapid and selective translational response 
of Arabidopsis plants upon activation of the effector-trig-
gered immunity (ETI) response. The authors found that, dur-
ing short intervals following ETI activation, the translational 
and transcriptional responses were uncoupled, especially for 
many of the genes that are negatively regulated. Accordingly, 
those genes with uncoupled transcription/translation showed 
the larger changes in translational efficiency upon activation 
of ETI. Genes involved in photosynthesis, gravi- and photo-
tropism, auxin metabolism and carbohydrate biosynthesis 
were down-regulated at the translational level, whereas genes 
that participate in cell wall thickness, secondary metabolism 
and cell death were translationally up-regulated, revealing a 
reprogramming of the host cells, which appear to undergo a 
switch from growth and development to defense (Box 2).
Box 1. TRAP-seq methodology
Pioneer translatome studies used ultracentrifugation through sucrose-density gradients to 
fractionate 40S and 60S ribosomal subunits, 80S monosomes and polyribosomes (polysomes) 
of different size (mRNAs with ≥2 ribosomes). Later on, a method based on affinity purification 
known as TRAP (Translating Ribosome Affinity Purification) was developed for plants (Zanetti 
et al., 2005), mammals (Heiman et al., 2008) and yeast (Halbeisen and Gerber, 2009). In plants, 
TRAP-seq is based on the expression of FLAG-tagged Ribosomal Protein Large subunit 18 
(RPL18), which is incorporated into translating ribosomes, providing a means of affinity-puri-
fying ribosomes, polysomes and associated mRNAs. The population of mRNAs present in 
TRAP samples is then analyzed by direct RNA sequencing. In parallel, total cellular mRNAs 
from the same tissue and conditions are analyzed by RNA-seq, thus allowing a comparison of 
transcriptional and translational changes in gene expression, as well as an estimation of the 
translational efficiency (the Log2 ratio of the amount of polysome-associated RNA to the total 
cellular amount of RNA for a given mRNA). More recently, a technique that precisely maps the 
ribosome-protected regions in an individual mRNA, known as ribosome footprinting or ribo-
some profiling (Ingolia et al., 2009), has been combined with TRAP and applied to gain insights 
into mechanistic aspects of translational control in plants (Juntawong et al., 2014).
 | 2079
A number of novel genes involved in plant immunity 
were identified through this translatomic analysis, including 
Phosphorylcholine cytidylyltransferase 2 (CCT2), the calos-
sin-like protein BIG, and CBL-Interacting protein kinase 5 
(CIPK5), and these were functionally validated by reverse 
genetics. Interestingly, Target of Rapamycin (TOR), which 
regulates plant development by restructuring cell growth and 
carbon/nitrogen metabolism (Ren et  al., 2012), dramatically 
decreased its translational efficiency upon activation of ETI. 
Moreover, Meteignier and co-workers showed that silencing 
TOR decreased plant susceptibility to the pathogenic bacterium 
Pseudomonas syringae and the oomycete Hyaloperonospora 
arabidopsidis, suggesting that TOR acts as a negative regula-
tor of disease resistance. Previous studies have shown that the 
transcriptome of plants with reduced TOR activity is enriched 
in transcripts involved in defense responses and innate immu-
nity, supporting the notion that TOR negatively regulates 
defense responses. This suggest that low levels of TOR are 
associated with reprogramming the growth-to-defense transi-
tion. In addition, reduction of TOR activity decreased anab-
olism and increased catabolism (Caldana et al., 2013), which 
might be linked to the reorientation of cellular activities to gen-
erate the energy required to mount a defense response.
The identification of  TOR as a negative regulator of 
plant immunity has novel implications concerning the 
similarities between plant and animal immune systems. 
In mammals, the TOR pathway integrates exogenous sig-
nals with endogenous cues such as cellular energy status, 
Box  2. Transcriptional and translational changes mediated by activation of NB-LRR 
receptors during the ETI response
Plant defense is based on two recognition systems. Pattern recognition receptors (PRRs) 
recognize pathogen-associated molecular patterns (PAMPs, such as the flagellin protein) to 
induce PAMP-triggered immunity (PTI), a level of defense that can be overcome by the pro-
duction of pathogen effectors, such as avrRpm1, which is produced by Pseudomonas syrin-
gae and introduced into the plant cell by the type III secretion system. The second layer of 
defense relies on the recognition of these effectors by receptors, such as the NB-LRR RPM1 
of Arabidopsis, triggering effector-triggered immunity (ETI), which induces a similar response 
to PTI, but more quickly and robustly. ETI can lead to the hypersensitive response (HR), a 
form of cell death limiting the spread of bio- and hemibio-trophic pathogens. Signaling events 
down-stream of receptor activation are poorly understood, but they include modulation of 
transcriptional responses in the nucleus. Meteignier et al. (2017) reveal that ETI also leads to 
changes in the translational status of pre-existing mRNAs in the cytoplasm. Translationally 
regulated mRNAs include those encoding HR-associated proteins, Target of Rapamycin (TOR) 
and other proteins such as Phosphorylcholine cytidylyltransferase 2 (CCT2), the calossin-like 
protein BIG and CBL-Interacting protein kinase 5 (CIPK5). TOR seems to affect the transition 
from growth to defense, whereas the other genes might act as positive or negative regulators 
of defense responses.
2080 |
hormones and growth factors to stimulate cell growth, pro-
liferation and differentiation. This pathway also plays a cen-
tral role in the translational control of  innate or adaptive 
immunity (Piccirillo et  al., 2014). The best-characterized 
translational targets of  TOR in mammals are 4E-binding 
proteins (4E-BPs), which act as translational suppressors 
by binding the eukaryotic initiation factor 4E (eIF4E, the 
cap-binding subunit of  the eIF4F complex), preventing the 
formation of  the eIF4F complex. The TOR–4EBPeIF4E 
module influences the translation of  a subset of  mRNAs 
referred to as ‘eIF4E sensitive’, including those encoding 
proteins involved in immunity, such as the transcription 
factor interferon regulatory factor 7 (IRF7). Mice defi-
cient in 4EBPs are less susceptible than the wild type to 
viral infection and unable to suppress the translation of 
the IRF7 transcript upon virus-induced inhibition of  TOR 
signaling (Colina et al., 2008). Although the translational 
targets of  TOR signaling in plants are not known yet, this 
pathway seems to play an active role in the switch from 
growth to immunity in both plants and mammals. Further 
studies are required to elucidate whether TOR influences 
the selective translation of  mRNAs during plant immunity 
and the potential targets of  translational control of  this 
pathway in plants.
Looking forward: mechanistic insights into 
translational control in plants
Most of  the high-throughput analyses have centered on the 
characterization of  transcriptomes, but application of  new 
techniques, such as TRAP-seq and Ribo-seq, have started 
to reveal the importance of  translation in the regulation of 
gene expression. The study of  Meteignier et al. nicely illus-
trates how the analysis of  translatomes might contribute to 
the identification of  new players with important functions 
in the adaptation and response of  plants to environmental 
challenges. Many biological processes could be fully under-
stood only through the characterization of  gene expression 
changes at different levels, complementing transcriptome 
studies with the analysis of  translatomes, ribosome foot-
prints, degradomes and proteomes. It is expected that the 
partial contribution of  each regulatory level will be differ-
ent for each process depending on the complexity and the 
time of  the response. Rapid responses, such as the hyper-
sensitive response, seem to rely on changes at the post-tran-
scriptional level, activating the translation of  pre-existing 
mRNAs that are stored inside the cell such that they are 
ready at the moment of  challenge, generating a functional 
protein in a short time-frame. In addition, it is necessary to 
study these processes in the individual cell types involved in 
the response, which can be achieved by combining TRAP 
with the use of  cell-specific promoters (Mustroph et  al., 
2009). Also, to understand better how genes are regulated 
at the translational level it will be crucial to identify the cis-
regulatory elements present in each transcript, as well as 
the trans-acting RNA-binding protein, which influence its 
selective association with the translational machinery and, 
more importantly, how its translational status can be mod-
ulated to generate the dynamic response required to adapt 
rapidly to changes in the environment. A preliminary study 
by Meteignier, Moffett and colleagues analyzing their candi-
dates for the presence of  shared elements in the untranslated 
regions is now available (Munusamy et al., 2017).
Key words: Effector-triggered immunity (ETI), NB-LRR proteins, plant 
defense, target of rapamycin (TOR), translation.
Journal of Experimental Botany, Vol. 68 No. 9 pp. 2077-2081, 2017  
doi: 10.1093/jxb/erx120
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Translational switching from growth to defense - a common role for TOR in plant and mammalian immunity?

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Translational switching from growth to defense - a common role for TOR in plant and mammalian immunity?

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