Organ-specific regulation of growth-defense tradeoffs by plants

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ScienceDirect Organ-specific regulation of growth-defense tradeoffs by plants Elwira Smakowska, Jixiang Kong, Wolfgang Busch and Youssef Belkhadir Plants grow while also defending themselves against phylogenetically unrelated pathogens. Because defense and growth are both costly programs, a plant’s success in colonizing resource-scarce environments requires tradeoffs between the two. Here, we summarize efforts aimed at understanding how plants use iterative tradeoffs to modulate differential organ growth when defenses are elicited. First, we focus on shoots to illustrate how light, in conjunction with the growth hormone gibberellin (GA) and the defense hormone jasmonic acid (JA), act to finely regulate defense and growth programs in this organ. Second, we expand on the regulation of growth-defense tradeoffs in the root, a less well-studied topic despite the critical role of this organ in acquiring resources in an environment deeply entrenched with disparate populations of microbes.

Thus, plants need to readily, yet precisely, appraise the resource investments needed to fend-off an attacker.

Address Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna Biocenter (VBC), Dr Bohr Gasse 3, Vienna 1030, Austria

The plant immune system is induced by the detection of evolutionary conserved microbe-associated molecular patterns (MAMPs) by cell surface proteins termed pattern recognition receptors (PRRs) [6]. Stereotypical plant PRRs includes the Receptor Like Kinases (RLKs) FLS2 [7], EFR [8], CERK1 [9], and the recently discovered lipopolysaccharide receptor LORE [10]. PRR activation results in the accumulation of reactive oxygen intermediates (ROIs), ion channel activation, and the activation of defense-specific MAPKs and CDPKs [11,12]. The activation of PRR signaling ultimately leads to a generic transcriptional response adapted to halt microbial proliferation with negligible fitness costs [2,13]. However, successfully evolving microbes stifle MAMPtriggered immunity (MTI) by either manipulating PRR signaling pathways or other defense-related components with effector proteins [14,15–18,19,20]. To counter this, plants have learned to monitor effector-activities by using a family of receptors termed NLRs [21,22]. NLRs survey various intracellular compartments and their activation upon effector detection unleashes a powerful immune response associated with significant fitness costs for the plant [23,24,25]. The activation of both MTI and NLR-mediated immunity at the single cell level leads to the redistribution of secondary messengers both locally and distally [26]. Moreover, the biosynthesis of the defense hormones salicylic acid (SA) and jasmonic acid (JA) during attack is a prerequisite for full disease resistance [27,28,29].

Corresponding author: Belkhadir, Youssef ([email protected])

Current Opinion in Plant Biology 2016, 29:129–137 This review comes from a themed issue on Growth and development Edited by Doris Wagner and Dolf Weijers

http://dx.doi.org/10.1016/j.pbi.2015.12.005 1369-5266/# 2015 Elsevier Ltd. All rights reserved.

Introduction Plants native to environments with scarce resources must optimize the partitioning of their supplies to grow [1]. Plants continuously monitor their environment for signals such as light, temperature, water, and nutrients to adequately partition their internal resources [1]. However, perpetual environmental changes necessitate constant readjustments of resources investments [2]. For instance, the presence of attackers near or on the plant body can further exacerbate ongoing conflicting resources demands for growth [2]. As such, plant responses to pathogen signals often require ‘trade-off’ processes in which resources initially dedicated to growth are diverted to sustain the high metabolic costs of defenses [3,4]. www.sciencedirect.com

The complexity of plants as environmental sensors is therefore critical when resource conflicts arise at the interface of defense and growth [2,5]. To this end, plants use sensory transduction systems that are able to appraise the ‘cost–benefit’ ratios of a given trade-off [5]. This review is motivated by fast-paced research programs aimed at deciphering how light signaling, growth-hormone networks, and defense systems intertwine to help plants arbitrate growth-defense conflicts (Table 1).

Design principles of plant defense systems

Light and photoreceptors are important modulators of growth-defense tradeoffs Environmental signals, such as temperature and light, can attenuate or exacerbate the capacity of a plant to mount an Current Opinion in Plant Biology 2016, 29:129–137

130 Growth and development

Table 1 Acronyms and names of regulatory components involved in the regulation of growth-defense trade-offs Name

Symbol

Protein function

BES1 BZR1

BRI1-EMS-suppressor 1 Brassinazole-resistant 1

Transcription factor Transcription factor

CDPKs

Calcium-dependent protein kinases

Kinase

CRY1

Cryptochrome 1

Photoreceptor

DELLAs

Transcriptional regulators

EFR

Family of proteins composed of: GA insensitive (GAI), repressor of ga1-3 (RGA), repressor of ga1-3-like protein 1 (RGL1), RGL2, and RGL3, Elongation factor-Tu receptor

FLS2

Flagellin sensing 2

HBI1

Homolog of BEE2 interacting with IHB1

Leucine-rich repeat serine/threonine receptor kinase Leucine-rich repeat serine/threonine receptor kinase Transcription factor

JAZs

Jasmonate ZIM-domain protein

Transcriptional regulators

LORE

S-locus lectin protein kinase

CERK1 MAPKs

Lipo oligosacharide-specific reduced elicitation Chitin elicitor receptor kinase 1 Mitogen-activated protein kinases

MYCs NINJA

Myelocytomatosis related proteins Novel interactor of JAZ

Transcription factor Transcriptional regulator

PhyA-B & PIFs

Phytochromes A and B & phytochromes interacting factors

Photoreceptor & transcription factors

TPL

TOPLESS

Transcriptional regulator

UVR8

UV-B photoreceptor 8/UVB-resistance 8

Photoreceptor

WRKYs

W-box DNA binding proteins

Transcription factors

NLRs

Nucleotide-binding domain leucine-rich repeat proteins

Intracellular receptors

LysM receptor like kinase Kinase

appropriate defense response [30,31]. A suite of highly specialized photoreceptor systems mediates plant responses to light. Their sequential activities during a photoperiod cycle allow plants to transduce different light qualities into differential growth responses in the shoot [32]. Amongst these receptors, the phytochromes have received much attention for their ability to modulate the high-order processes of SA-controlled and JA-controlled defenses [33,34,35]. Briefly, attenuated immune responses to the fungal pathogen Fusarium oxysporum or to the bacterium Current Opinion in Plant Biology 2016, 29:129–137

Description Transcription factors acting as master regulators of brassinosteroids transcriptional programs. Intracellular kinases sensitive to Calcium variation in the cystosol. CRY1 senses variation in the blue-green ratio of light. DELLAs are plant growth regulators whose degradation is promoted by the phytohormone gibberellin (GA). Act as a pattern-recognition receptor for the bacterial MAMPs elongation factor Tu. Act as a pattern-recognition receptor for the conserved flg22 epitope of the bacterial flagellum. Central growth component involved in a complex regulation circuit. Functions as a major node to mediate a trade-off between BRs and immunity. Key integrators of the jasmonate (JA) signaling pathway. Involved in lipopolysaccharide (LPS) sensing. Involved in chitin perception and signaling. MAPK signaling cascades gate the transmission of extracellular signals to downstream nuclear effectors by sequential phosphorylation. Important MAPKs involved in plant immunity include: MPK3, MPK4 and MPK6. Key mediators of jasmonate signaling. NINJA functions as a negative regulator of JA responses. Basic helix-loop-helix (bHLH) containing transcription factors involved in cellular elongation TPL functions as a negative regulators of JA responses Orchestrate the transcriptional programs during UV exposure. Act in a complex network to regulate the amplitude of defense responses. WRKYs can act as positive and negative regulators of plant immunity Also known as R genes, NLRs monitor the intracellular environment for the presence of pathogen effectors.

Pseudomonas syringae have been reported in Arabidopsis phyA and phyB mutant plants [36]. Similarly, under continuous light, the blue light receptor CRY1 positively modulate NLR-mediated disease resistance [37]. Finally, Arabidopsis immunity against Botrytis cinerea also requires UV-B absorption by the photoreceptor UVR8 [38,39]. While these important studies have demonstrated that light quality and quantity can significantly modulate the outcome of a plant-pathogen interaction, the molecular mechanisms that allow plants to set light receptors sensitivity to a www.sciencedirect.com

Tradeoffs between growth and plant defense Smakowska et al. 131

particular range for optimal growth and defenses are still poorly understood. Mechanistic insights have surfaced from seminal studies focusing on variations in the ratio of red to far-red light (R:FR) [35,40]. Plants monitor R:FR light to anticipate competition between neighboring plants [41]. Plants growing in low R:FR light try to overgrow their competitors by positioning their photosynthetic leaves in more favorable light conditions. This response, called the shade avoidance syndrome (SAS), is triggered by the accumulation of inactive PhyB molecules [42,43], which in turn allows members of the PIF family to recruit the cell elongation machinery to boost the SAS response [44] (Figure 1). Thus, developmental plasticity to SAS requires resource allocation alterations, which in turn can limit investment in defense. The reduction of ‘active’ PhyB intermediates due to low R:FR ratios negatively regulates the induction of SA and JA signaling, thereby reducing the concentrations of defenses metabolites [34,45]. Desensitization of JA signaling during SAS occurs through the stabilization of the transcriptional repressor JAZs and the accumulation of the transcriptional activators MYCs through an unknown mechanism [36,46] (Figure 1). In the absence of JA, JAZs acts as key repressors of JA signaling by sequestering the transcriptional activators MYCs [47,48,49,50] (Figure 1). The destabilization of JAZs in the presence of elevated concentrations of JA is therefore necessary for JA-dependent responses to occur [46]. SA and JA signaling are also subjected to antagonistic and synergistic relationships with many other phytohormones [51]. These modulatory relationships have been extensively reviewed over the past years and excellent literature is available [5,52–54]. Amongst others, the modulator relationships between brassinosteroids (BRs) and MTI together with the nexus between GA and JA exquisitely illustrate how plants manage to mechanistically balance immunity and growth when pathogen signals are detected.

BR signaling impacts transcriptional networks involved in growth and immunity BR biosynthetic genes are down regulated during MTI because BR signals can prioritize growth over defense [55– 57,58]. Elevated BR signaling leads to the suppression of MTI through the master regulators BZR1 and BES1 [59,60]. BZR1 does so by promoting the expression of several WRKY transcription factors that negatively regulate early MAMP triggered defenses [59]. To this end, BZR1 can interact with WRKY40, a known negative regulator of defense [59]. Atop this regulatory layer, BZR1 acts in concert with HBI1, another bHLH protein, to form a positive feed-forward loop that balances BR-modulated growth and MTI [61,62]. In contrast to BZR1, BES1 is phosphorylated by MPK6 to promote defense [61]. Thus, BES1 and BZR1 are important regulatory decision-making www.sciencedirect.com

nodes that integrate BR signals on MTI, and hence regulate growth-defense tradeoffs. It remains unclear how the balanced and overlapping activities of BZR1 and BES1 during BR-dependent growth antagonistically modulate MTI at the transcriptional level. Since BRs signaling controls the flux of the GA biosynthetic pathway during growth, it is likely that these two hormones also intersect during defenses [63]. Accordingly, the BR-dependent prioritization of growth over defense is quite potent in dark-grown etiolated seedlings, suggesting the requirement of other signaling pathways involving light and likely GA [53,59].

GA and JA: a paradigm of signal integration at the growth-defense nexus GA influences plant growth and defense by targeting for degradation a class of GA-controlled inhibitory proteins, called DELLAs [44,64,65] (Figure 1). DELLAs can act as key negative regulatory switches at the interface of growth and defense by simultaneously integrating light and JA signals [66,67]. On the one hand, DELLAs selectively interact with JAZs to regulate their distribution to, and sequestering effects on, MYC transcription factors [67,68] (Figure 1). On the other hand, DELLAs also interacts with PIFs to interfere with their transcriptional activities during photomorphogenesis or SAS [66,69] (Figure 1). In addition, DELLAs can also interact with MYCs [70], and MYCs in return regulate the transcription of DELLAs [71]. By inducing the degradation of DELLAs, elevated GA levels have two immediate effects. First, JAZs escape DELLA-dependent sequestration, which in turn allows JAZs to freely associate with MYCs to lower the transcriptional output of the JA pathway [46,47] (Figure 1). Second, PIFs are no longer sequestered by DELLAs and can therefore freely reach the promoter of their target genes to control specific growth programs (Figure 1). Conversely, lowered GA concentrations alleviate the cumulative negative regulatory effects of JAZ on MYC-controlled transcription, hence promoting defenses and reducing growth (Figure 1). Moreover, during pathogen attack, the induction of JA signaling can further prioritize defense over growth by enhancing the sequestration of PIFs by DELLAs [72] (Figure 1). In sum, the combinatorial interactions among PIFs, DELLAs and JAZs form a transcriptionally centered ‘hub’ that can act to finely orchestrate growth-defense tradeoffs [73]. To add another layer of complexity, the respective sets of receptors and corresponding transcription factors are redundantly encoded in light, JA and GA signaling. Understanding how this redundancy fine-tunes the stoichiometry and the dynamic continuum of this ‘transcriptional hub’ in an organ-specific fashion is a question of paramount interest. To date, we still lack detailed knowledge of how JA and GA interact to remodel the constituent tissues of the root Current Opinion in Plant Biology 2016, 29:129–137

132 Growth and development

Figure 1

(a)

(b) PhyB

R:FR PIFs PhyB

PIFs

PIFs

PIFs

Pathogens

Pathogens

Rested Hub

JA

GA

JA

GA

GA

DELLA JAZ

DELLA

?

Activated Hub

JA DELLA

PIFs PIFs

MYC

DELLA

PIFs JAZ

PIFs

SAS-target genes

MYC

GA-target genes

DEFENSE

DELLA

MYC MYC

JA-target genes

GA-target genes

GROWTH

DEFENSE

JA JAZ

JAZ

MYC

PIFs

GA

DELLA

JAZ

PIFs

JAZ

?

GA-target genes

JA-target genes

JA-target genes

DEFENSE

GROWTH

SAS-target genes

PIFs

PIFs

JAZ

MYC

GA-target genes

DEFENSE

JA-target genes

GROWTH

GROWTH

(c) MYC3 NINJA

TPL

JAZ MYC

JAZ peptide

JA-target genes

GA

?

JA Current Opinion in Plant Biology

Snapshots of growth-defense tradeoffs regulation by Light, GA and JA. (a) In normal light conditions, a signal-competent, yet rested, transcriptional hub composed of DELLA, PIFs, JAZ, and MYC is kept in check by ‘trans’ mechanisms. Please note that the depiction of the hub in our figure is hypothetical as there are no direct evidences that these four proteins exist in the same protein complex. Increase in GA concentrations leads to the degradation of DELLAs, which triggers the dissociation of PIFs, JAZ, and MYCs (left panel). PIFs, either on their own or together with other transcription factors, bind their target promoters to activate the expression of thousands of genes for optimal GA-regulated growth. Meanwhile, JAZs sequester MYCs proteins to block their DNA binding and transcriptional activities. By acting as a balance scale (lower panel), plants weight GA signals to prioritize growth over defenses. When pathogens are present in the ambient environment JA levels increase (right panel). This in turn leads to the degradation of JAZs, which triggers the dissociation of DELLAs, PIFs, and MYCs. MYCs bind their target promoters to activate the expression of genes required for JA-regulated defenses. Meanwhile, the sequestration of PIFs by DELLAs prevents the unfolding of GA-controlled growth programs. Once more, by acting like a balance scale (lower panel), plants prioritize defense over growth by integrating JA signals. (b) Under low red: far red (R:FR), PhyB levels decrease leading to an increased accumulation of PIFs. The endogenous levels of GA together with PIFs accumulation dramatically enhance cellular elongation required for the SAS responses (Left panel). Meanwhile JAZs still sequester MYCs proteins to block their DNA transcriptional activities. By acting like a balance scale (lower panel), plants weight GA and low R:FR signals to boost growth at the cost of defenses. JA levels increase upon pathogen detection (right panel). However low R:FR antagonize JA accumulation by 1 — stabilizing the JAZs and 2 — destabilizing the MYCs. As such, MYCs can no longer activate their target genes and consequently the output of JA-regulated defenses is lowered. The destabilization of JAZs free up DELLAs for PIFs sequestration. However, elevated PIFs levels in R:FR conditions outcompete these sequestering effects and SAS-mediated growth occurs, albeit not as efficiently as in the absence of pathogens. By acting like a balance scale (lower panel), plants try to prioritize defense over growth but R:FR light overrides the initial program. The question mark highlights knowledge gaps in the signaling pathway. (c) A model of regulation of basal JA signaling by NINJA in the roots. Like in the shoot, the molecular basis of JA signaling regulation relies on the sequestration of MYCs by JAZs. However NINJA positively regulates root growth in the absence of pathogen signals. The left panel shows the structural basis of MYC3 inhibition by a JAZ peptide.

Current Opinion in Plant Biology 2016, 29:129–137

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Tradeoffs between growth and plant defense Smakowska et al. 133

when defenses are elicited. The predominant function of NINJA in mediating JA-dependent responses in the roots suggests that the regulation of the JA pathway can differ in many aspects within the same plant [74,75] (Figure 1c). Moreover, the sites of JA and GA accumulation in the root can also hinder the regulation of growthdefense tradeoffs in this organ. The recent in vivo implementation of the JA biosensor ‘Jas9-VENUS’ in Arabidopsis revealed peaks of maximal accumulation for JA in the epidermis, ground tissues and vascular tissues [76]. In stark contrast, fluorescently labeled GAs signal and accumulate specifically in the endodermal cells of the root elongation zone [77,78]. As such, the organizational principles of JA and GA actions on growth and defense in the root are expected to radically diverge from the conceptual paradigms derived from the shoot. Therefore, understanding the principles of the JA-GA crosstalk in the root represents an ambitious goal open to investigation.

Regulation of growth-defense tradeoffs in the root necessitates multilayered decisionmaking systems In roots, decisions originating at the single cell level can impact the overall growth and defense systems of aboveground tissues [79]. Root immunity has been extensively studied in the context of plant–nematode interactions [80]. In a way reminiscent to MAMPs, pheromones (e.g. ascarosides) produced by various genera of nematodes can induce plant defenses and, in some cases, even help roots resist infection by other pathogens [80,81]. Interestingly, defense priming by ‘ascarosides’ in roots and shoots seems to be dosage dependent [81]. Thus, nematodes are likely to be perceived by organ-specific mechanisms that display different activation thresholds. In agreement with this hypothesis, defenses against the cyst nematode Heterodera schachtii require differential JA and SA responses in roots and shoots [82–84]. The colonization of root cells by plant growth promoting microbes (PGPMs) also primes the entire plant immune system for rapid deployment against a broad range of pathogens [85]. This ‘priming’ is called induced systemic resistance (ISR) and requires an intact JA pathway [86]. In contrast to leaves, the relationship between PRRs and NLRs sensors is largely uncharacterized in roots [87]. Pioneering studies have demonstrated that FLS2 preferentially responds to its ligand (flg22) in the root elongation zone [88], but at the transcriptional level FLS2 seems to be highly expressed in the inner cell layers and in the vascular cylinder [89]. A very elegant study by Wyrsch et al. has demonstrated that FLS2 function in the root is not correlated with its basal transcriptional patterns [90]. Rather, functional complementation assays of the fls2 mutant with tissue-specific expression ‘cassettes’ driving the expression of FLS2 have demonstrated a sectorial requirement for sustained signaling [90]. These www.sciencedirect.com

differential sector activities perhaps allow the root to finely discriminate pathogens from mutualists and commensals for zone-specific confinement. Ultimately this strategy would allow roots to tolerate specific levels of colonization by beneficial and/or detrimental microbes when differential growth needs to occur [91]. The specific, yet relative, cellular distribution of PRRs and NLRs signaling systems could therefore constrain the regulation of growth-defense tradeoffs in the root. Atop this proposed regulatory layer, the landmark study by Lebeis et al. suggests that the endogenous rates of SA biosynthesis in various cell-types could readily prioritize growth or defense by shaping the diversity of root-inhabiting microbial communities [92]. All in all, new conceptual frameworks are needed to understand how growth and defense occur simultaneously in the root and the emerging studies on the rhizosphere microbiome have the potential to bolster our understanding of the regulation of growth-defense trade-offs in this organ [87,93,94,95]. Here, we posit that the regulation of defenses in the root will rely on three overlapping mechanisms ranging from avoidance, tolerance to resistance. Moreover, we propose that the regulation of growth-defense tradeoffs in roots can be quantitatively modulated depending on the mechanism at play. Roots can anticipate the encounter of microbe niches by detecting chemicals derived from microbial metabolism [79]. Thus, the root avoidance strategy, which requires a risk-assessment of microbe exposure before infection, will actively prioritize growth away from zones of highpathogen density. In such a scenario, the involvement of hormonal pathways controlling defense and growth could play a major role in adjusting root growth rates and growth angles based on microbial cues [96]. However, both beneficial and detrimental microbes often occur together in the soil. Thus, to reach out to PGPMs, roots will often rely on tolerance mechanisms [79]. Despite their crucial roles, very little is known about the full array of tolerance mechanisms roots can employ. The emerging paradigms for tolerance put forth that pathogens, mutualists, and commensals are all equally challenged by the root immune system [97,98]. Hence, successful microbial colonization should largely depend on the immunosuppressive abilities of a given microbe [98]. Finally, elimination of pathogens in the root will rely on resistance mechanisms accompanied by major collateral tissue damage. In this case, we envision that the balance of tolerance and resistance will be pathogen-specific and that the specific resources being competed for will favor tolerance for one microbe while promoting resistance against another. In this model, tolerance mechanisms can operate to limit the tissue damage inflicted by resistance, thereby allowing for a higher amplitude and extent Current Opinion in Plant Biology 2016, 29:129–137

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of the immune response than would have otherwise been possible. Finally, the tolerance capacity will depend on the tissue repair capacity and the cellular renewal rates of the stem cell niches [99].

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Concluding remarks To conclude, the internal programs that regulate major developmental transitions and defenses in plants involve the collaborative actions of many small molecule hormones and light. Despite the considerable amount of work describing the influence of light and hormones on growth defense tradeoffs in the shoot, a set of fascinating biological questions remains unanswered in the root. The less well-characterized principles of root defense systems together with the inherent complexity of root growth will make it challenging to understand the regulation of growth-defense tradeoffs in this organ. Large-scale quantitative genetic studies that systematically query root responses to molecules derived from microorganisms and/or microorganisms themselves will be instrumental in addressing this challenge [100,101]. Tremendous progress in this area is to be expected as many high-throughput root phenotyping systems have been developed in which these interactions can be monitored at different scales (e.g. cellular, tissue, and whole root level) [102– 105]. Importantly, the above mentioned phenotyping pipelines and quantitative genetics approaches can be implemented in other plant systems, such as arbuscular mycorrhiza forming plants that represent 70–90% of the more than three hundred thousand species of land plants that inhabit our planet.

Acknowledgements This work was supported by funds from the Austrian Academy of Science (OEAW) through the Gregor Mendel Institute (Y.B and W.B). We would like to thank Mark Talbot (Commonwealth Scientific and Industrial Research Organisation (CSIRO)) for providing electron scan pictures of the Arabidopsis seedling used in Figure 1.

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10. Ranf S, Gisch N, Schaffer M, Illig T, Westphal L, Knirel YA,  Sanchez-Carballo PM, Zahringer U, Huckelhoven R, Lee J et al.: A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat Immunol 2015, 16:426-433. This oustanding article report on the discovery of the long sought LPS receptor in plants. A must read! 11. Macho AP, Zipfel C: Plant PRRs and the activation of innate immune signaling. Mol Cell 2014, 54:263-272. 12. Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A,  Segonzac C, Malinovsky FG, Rathjen JP, MacLean D, Romeis T et al.: The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 2014, 16:605-615. This excellent study report the discovery of a calcium-dependent kinase involved in the regulation of MAMP triggered immunity. CPK28 targets the master regulator BIK1 to regulate its availability during PRR signaling. 13. Dangl JL, Horvath DM, Staskawicz BJ: Pivoting the plant immune system from dissection to deployment. Science 2013, 341:746-751. 14. Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C,  Roy S, Kadota Y, Oh MH, Sklenar J, Derbyshire P et al.: A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 2014, 343:1509-1512. A scintillating paper showing that the PRR EFR can be negatively regulated through effector-mediated tyrosine dephosphorylation. This is a landmark study! 15. Macho AP, Zipfel C: Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr Opin Microbiol 2015, 23:14-22. 16. Lozano-Duran R, Bourdais G, He SY, Robatzek S: The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol 2014, 202:259-269. 17. Lewis JD, Wilton M, Mott GA, Lu W, Hassan JA, Guttman DS, Desveaux D: Immunomodulation by the Pseudomonas syringae HopZ type III effector family in Arabidopsis. PLOS ONE 2014, 9:e116152. 18. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT et al.: Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 2011, 333:596-601. 19. Wessling R, Epple P, Altmann S, He Y, Yang L, Henz SR,  McDonald N, Wiley K, Bader KC, Glasser C et al.: Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 2014, 16:364-375. The findings presented in this paper underscore the evolutionary constraints that pathogen from different phyla have to overcome to become successful. Independently evolved effectors from the eubacterial pathogen Pseudomonas syringae and the oomycete pathogen Hyaloperonospera arabidopsidis are shown to target predominantly a common set of host physiological targets and networks proteins in Arabidopsis. 20. Cheng Z, Li JF, Niu Y, Zhang XC, Woody OZ, Xiong Y, Djonovic S,  Millet Y, Bush J, McConkey BJ et al.: Pathogen-secreted proteases activate a novel plant immune pathway. Nature 2015, 521:213-216. This research shows that Pseudomonas aeruginosa is able to secrete a bacterial protease to activate a signalling pathway involving the subunits of an heterotrimeric G-protein complexes, functionning upstream of a www.sciencedirect.com

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MAPK module. Another scintillating example of effector manipulation of plant signaling pathways. 21. Jacob F, Vernaldi S, Maekawa T: Evolution and conservation of plant NLR functions. Front Immunol 2013, 4:297. 22. Li X, Kapos P, Zhang Y: NLRs in plants. Curr Opin Immunol 2015, 32:114-121. 23. Chung EH, El-Kasmi F, He Y, Loehr A, Dangl JL: A plant  phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 2014, 16:484-494. 13 years after its discovery, the protein RIN4 is still the subject of very exciting discoveries! The authors build on previous work to show that the sequential order in which RIN4 is phosphorylated is critical to ultimately trigger NLR-based immunity. 24. Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D,  Kraut A, Zhou B, Levaillant M, Adachi H, Yoshioka H et al.: A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 2015, 161:1074-1088. The manuscript presents new paradigms of NLR-mediated signal transduction. The studies show that twinned NLRs have incorporated decoy domains that structurally mimic pathogen virulence targets to monitor effector activities and launch a powerful immune response. 25. Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J,  Derbyshire P, Cevik V, Rallapalli G, Saucet SB et al.: A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 2015, 161:1089-1100. See annotation to Ref. [24]. 26. Fu ZQ, Dong X: Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 2013, 64: 839-863. 27. Zheng XY, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW, Kay SA, Dong X: Spatial and temporal regulation of biosynthesis of the  plant immune signal salicylic acid. Proc Natl Acad Sci U S A 2015, 112:9166-9173. SA biosynthesis is essential for local and systemic defenses. Here the authors demonstrate that the SA biosynthetic pathway is regulated spatially and temporally by two newly identified transcription factors. 28. de Torres Zabala M, Zhai B, Jayaraman S, Eleftheriadou G, Winsbury R, Yang R, Truman W, Tang S, Smirnoff N, Grant M:  Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection. New Phytol 2015. An important paper that challenges our current understanding of how SA and JA signaling work. 29. Caarls L, Pieterse CM, Van Wees SC: How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 2015, 6:170. 30. Alcazar R, Parker JE: The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci 2011, 16:666-675. 31. Hua J: Modulation of plant immunity by light, circadian rhythm, and temperature. Curr Opin Plant Biol 2013, 16:406-413. 32. Fankhauser C, Christie JM: Plant phototropic growth. Curr Biol 2015, 25:R384-R389. 33. Ballare CL: Light regulation of plant defense. Annu Rev Plant Biol 2014, 65:335-363. 34. Cargnel MD, Demkura PV, Ballare CL: Linking phytochrome to plant immunity: low red: far-red ratios increase Arabidopsis  susceptibility to Botrytis cinerea by reducing the biosynthesis of indolic glucosinolates and camalexin. New Phytol 2014, 204:342-354. A seminal study showing that low R:FR light affect defenses against a necrotroph. 35. Moreno JE, Ballare CL: Phytochrome regulation of plant immunity in vegetation canopies. J Chem Ecol 2014, 40:848857. 36. Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M,  Patitucci MS, Pierik R, Pieterse CM, Ballare CL: Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and www.sciencedirect.com

jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol 2012, 158: 2042-2052. Another seminal study showing that low R:FR light affect specifically the higher order of defenses through the key protein JAZ10. 37. Wu L, Yang HQ: CRYPTOCHROME 1 is implicated in promoting R protein-mediated plant resistance to Pseudomonas syringae in Arabidopsis. Mol Plant 2010, 3:539-548. 38. Demkura PV, Ballare CL: UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Mol Plant 2012, 5:642-652. 39. Mazza CA, Ballare CL: Photoreceptors UVR8 and phytochrome  B cooperate to optimize plant growth and defense in patchy canopies. New Phytol 2015, 207:4-9. This excellent research builds on previous work to show that Red and Far red light together with UVB radiation influence plant growth and defenses. 40. Martinez-Garcia JF, Gallemi M, Molina-Contreras MJ, Llorente B, Bevilaqua MR, Quail PH: The shade avoidance syndrome in Arabidopsis: the antagonistic role of phytochrome a and B differentiates vegetation proximity and canopy shade. PLOS ONE 2014, 9:e109275. 41. Keller MM, Jaillais Y, Pedmale UV, Moreno JE, Chory J, Ballare CL: Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. Plant J 2011, 67:195-207. 42. Burgie ES, Bussell AN, Walker JM, Dubiel K, Vierstra RD: Crystal  structure of the photosensing module from a red/far-red lightabsorbing plant phytochrome. Proc Natl Acad Sci U S A 2014, 111:10179-10184. This work is a landmark in the field of plant photobiology. The authors present the structure of the light sensing domain of Phytochrome B. This study is however begging for the crystalization and 3D resolution of a full phytochrome protein in its rested and activated forms. 43. Burgie ES, Vierstra RD: Phytochromes: an atomic perspective on photoactivation and signaling. Plant Cell 2014, 26: 4568-4583. 44. Jaillais Y, Vert G: Brassinosteroids, gibberellins and lightmediated signalling are the three-way controls of plant sprouting. Nat Cell Biol 2012, 14:788-790. 45. de Wit M, Spoel SH, Sanchez-Perez GF, Gommers CM, Pieterse CM, Voesenek LA, Pierik R: Perception of low red:farred ratio compromises both salicylic acid- and jasmonic aciddependent pathogen defences in Arabidopsis. Plant J 2013, 75:90-103. 46. Chico JM, Fernandez-Barbero G, Chini A, Fernandez-Calvo P,  Diez-Diaz M, Solano R: Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis. Plant Cell 2014, 26:1967-1980. Excellent work showing that low R:FR light has a dual action on JA signaling. 47. Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM et al.: The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 2011, 23:701-715. 48. Kazan K, Manners JM: MYC2: the master in action. Mol Plant 2013, 6:686-703. 49. Zhang F, Yao J, Ke J, Zhang L, Lam VQ, Xin XF, Zhou XE, Chen J,  Brunzelle J, Griffin PR et al.: Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature 2015, 525:269-273. Spectacular work that helps rationalize a decade of forward genetic and molecular studies aimed at understanding the mechanisms underlying JAZ repression of MYC transcription factors. 50. Goossens J, Swinnen G, Vanden Bossche R, Pauwels L, Goossens A: Change of a conserved amino acid in the MYC2 and MYC3 transcription factors leads to release of JAZ repression and increased activity. New Phytol 2015, 206: 1229-1237. Current Opinion in Plant Biology 2016, 29:129–137

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51. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC: Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 2012, 28:489-521. 52. Vos IA, Moritz L, Pieterse CM, Van Wees SC: Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions. Front Plant Sci 2015, 6:639. 53. Lozano-Duran R, Zipfel C: Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci 2015, 20:12-19. 54. Spoel SH, Johnson JS, Dong X: Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 2007, 104:18842-18847.

66. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY: Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 2012, 14:810-817. 67. Hou X, Lee LY, Xia K, Yan Y, Yu H: DELLAs modulate jasmonate  signaling via competitive binding toJAZs. Dev Cell 2010, 19:884-894. This work shows that DELLAs and JAZs can act together to allow synergy between GA and JA signaling in the control of hypocotyl, seedling and trichome development. However different mechanisms seem to be at play. The latter reinforces our hypothesis that growth-defense tradeoff regulation by GA and JA is also likely to be regulated in a tissue-specific manner.

55. Belkhadir Y, Jaillais Y, Epple P, Balsemao-Pires E, Dangl JL, Chory J: Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci U S A 2012, 109:297-302.

68. Qi T, Huang H, Wu D, Yan J, Qi Y, Song S, Xie D: Arabidopsis  DELLA and JAZ proteins bind the WD repeat/bHLH/MYB complex to modulate gibberellin and jasmonate signaling synergy. Plant Cell 2014, 26:1118-1133. See annotation to Ref. [67].

56. Jaillais Y, Belkhadir Y, Balsemao-Pires E, Dangl JL, Chory J: Extracellular leucine-rich repeats as a platform for receptor/ coreceptor complex formation. Proc Natl Acad Sci U S A 2011, 108:8503-8507.

69. Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY: Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 2014:e03031.

57. Albrecht C, Boutrot F, Segonzac C, Schwessinger B, GimenezIbanez S, Chinchilla D, Rathjen JP, de Vries SC, Zipfel C: Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci U S A 2012, 109: 303-308.

70. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY: Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 2012, 24:2635-2648.

58. Jimenez-Gongora T, Kim SK, Lozano-Duran R, Zipfel C: Flg22 triggered immunity negatively regulates key BR biosynthetic genes. Front Plant Sci 2015, 6:981. Extremely interesting report suggesting that MTI and BRs can inhibit each other. 59. Lozano-Duran R, Macho AP, Boutrot F, Segonzac C, Somssich IE,  Zipfel C: The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. Elife 2013, 2:e00983. In this manuscript the author demonstrate that BR signaling and MTI intersect at the level of the transcription factor BZR1. The findings reported here challenge the models of BR inhibition of defenses (see Ref. [55]). 60. Kang S, Yang F, Li L, Chen H, Chen S, Zhang J: The Arabidopsis  transcription factor brassinosteroid insensitive1-ethyl methanesulfonate-suppressor1 is a direct substrate of mitogen-activated protein kinase6 and regulates immunity. Plant Physiol 2015, 167:1076-1086. This paper implicates BES1 in the regulation of defenses. The authors demonstrate that BES1 phosphorylation by MAPK6 is a requisite to promote defenses. 61. Malinovsky FG, Batoux M, Schwessinger B, Youn JH, Stransfeld L,  Win J, Kim SK, Zipfel C: Antagonistic regulation of growth and immunity by the Arabidopsis basic helix-loop-helix transcription factor homolog of brassinosteroid enhanced expression2 interacting with increased leaf inclination1 binding bHLH1. Plant Physiol 2014, 164:1443-1455. 62. Fan M, Bai MY, Kim JG, Wang T, Oh E, Chen L, Park CH, Son SH,  Kim SK, Mudgett MB et al.: The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogenassociated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 2014, 26:828-841. This reference together with [61] shows that BR and MTI also intersect at the transcriptionnal level via the bHLH protein HBI1. 63. Unterholzner SJ, Rozhon W, Papacek M, Ciomas J, Lange T,  Kugler KG, Mayer KF, Sieberer T: Poppenberger B: brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell 2015, 27:2261-2272. This very nice piece of work demonstrates that BRs can reprogram the GA biosynthetic pathway.

71. Wild M, Daviere JM, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P: The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 2012, 24:3307-3319. 72. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW et al.: Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci U S A 2012, 109:E1192-E1200. 73. Pieterse CM, Pierik R, Van Wees SC: Different shades of JAZ during plant growth and defense. New Phytol 2014, 204: 261-264. 74. Acosta IF, Gasperini D, Chetelat A, Stolz S, Santuari L, Farmer EE:  Role of NINJA in root jasmonate signaling. Proc Natl Acad Sci U S A 2013, 110:15473-15478. A much awaited article that further investigates the root specific functions of NINJAs. The authors show that NINJA is a negative regulator of JA signaling in the root and by acting so, NINJA activities control cellular elongation in this organ. 75. Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Perez AC, Chico JM, Bossche RV, Sewell J, Gil E et al.: NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 2010, 464:788-791. 76. Larrieu A, Champion A, Legrand J, Lavenus J, Mast D, Brunoud G,  Oh J, Guyomarc’h S, Pizot M, Farmer EE et al.: A fluorescent hormone biosensor reveals the dynamics of jasmonate signalling in plants. Nat Commun 2015, 6:6043. Inspiring work that reports on the implementation of a JA biosensor in Arabidopsis roots. Using their biosensor, the authors show that JA accumulates in both epidermal cells and the inner layers. More work of this type is needed to understand how phytohormones distribute in plant cells. 77. Shani E, Weinstain R, Zhang Y, Castillejo C, Kaiserli E, Chory J,  Tsien RY, Estelle M: Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc Natl Acad Sci U S A 2013, 110:4834-4839. In this work the authors show that active GA accumulates in the endodermis. This work is consistent with previously published information [84]. Though very nice, this work is begging for the engineering and implementation of a GA biosensor.

64. Jaillais Y, Chory J: Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 2010, 17:642-645.

78. Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT, Hedden P, Bhalerao R, Bennett MJ: Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 2008, 10:625-628.

65. Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JD: DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 2008, 18:650-655.

79. Zamioudis C, Korteland J, Van Pelt JA, van Hamersveld M, Dombrowski N, Bai Y, Hanson J, Van Verk MC, Ling HQ, SchulzeLefert P et al.: Rhizobacterial volatiles and photosynthesisrelated signals coordinate MYB72 in Arabidopsis roots during

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onset of induced systemic resistance and iron deficiency responses. Plant J 2015. 80. Goverse A, Smant G: The activation and suppression of plant innate immunity by parasitic nematodes. Annu Rev Phytopathol 2014, 52:243-265. 81. Manosalva P, Manohar M, von Reuss SH, Chen S, Koch A,  Kaplan F, Choe A, Micikas RJ, Wang X, Kogel KH et al.: Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nat Commun 2015, 6:7795. Excellent work that shows that small molecules synthesized by nematodes can act in a way reminiscent to that or MAMPs. 82. Nguyen PD, Pike S, Wang J, Nepal Poudel A, Heinz R, Schultz JC, Koo AJ, Mitchum MG, Appel HM, Gassmann W: The Arabidopsis immune regulator SRFR1 dampens defences against herbivory by Spodoptera exigua and parasitism by Heterodera schachtii. Mol Plant Pathol 2015. 83. Kammerhofer N, Radakovic Z, Regis JM, Dobrev P, Vankova R, Grundler FM, Siddique S, Hofmann J, Wieczorek K: Role of stress-related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytol 2015, 207:778-789. 84. Nahar K, Kyndt T, De Vleesschauwer D, Hofte M, Gheysen G: The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 2011, 157:305-316. 85. Zamioudis C, Hanson J, Pieterse CM: beta-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. New Phytol 2014, 204:368-379. 86. Ton J, De Vos M, Robben C, Buchala A, Metraux JP, Van Loon LC, Pieterse CM: Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 2002, 29:11-21. 87. Hacquard S, Garrido-Oter R, Gonzalez A, Spaepen S, Ackermann G, Lebeis S, McHardy AC, Dangl JL, Knight R, Ley R et al.: Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 2015, 17:603-616. 88. Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, WerckReichhart D, Ausubel FM: Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 2010, 22:973-990. 89. Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A, Boller T,  Robatzek S: Expression patterns of flagellin sensing 2 map to bacterial entry sites in plant shoots and roots. J Exp Bot 2014, 65:6487-6498. The manuscript presents pioneering work aimed at understanding how MTI is regulated in different root tissues. The authors show that both, transcriptionnal and posttranscriptionnal mechanisms regulate FLS2 distribution and function in root cells. 90. Wyrsch I, Dominguez-Ferreras A, Geldner N, Boller T: Tissue specific FLAGELLIN-SENSING 2 (FLS2) expression in roots restores immune responses in Arabidopsis fls2 mutants. New Phytol 2015, 206:774-784. See annotation to Ref. [89]. 91. Zamioudis C, Pieterse CM: Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 2012, 25:139150. 92. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J,  McDonald M, Malfatti S, Glavina del Rio T, Jones CD, Tringe SG et al.: Plant microbiome. Salicylic acid modulates colonization

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of the root microbiome by specific bacterial taxa. Science 2015, 349:860-864. Seminal work demonstrating the importance of SA biosynthesis for the composition of root microbiomes. Using conventional SA Arabidopsis mutants in conjunction with synthetic bacterial communities the authors demonstrate that the balance of bacterial families that accumulate around or inside a root is regulated by the levels of SA. A must read! 93. Bulgarelli D, Garrido-Oter R, Munch PC, Weiman A, Droge J, Pan Y, McHardy AC, Schulze-Lefert P: Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 2015, 17:392-403. 94. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E et al.: Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 2012, 488:91-95. 95. Berendsen RL, van Verk MC, Stringlis IA, Zamioudis C,  Tommassen J, Pieterse CM, Bakker PA: Unearthing the genomes of plant-beneficial Pseudomonas model strains WCS358, WCS374 and WCS417. BMC Genomics 2015, 16:539. Very important work reporting for the first time on the genomes of Pseudomonas fluorescens strains that are commonly used to understand the various functions of the root immune system. 96. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM: Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 2013, 162:304-318. 97. Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel KH, Schafer P: Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 2011, 156:726-740. 98. Lakshmanan V, Kitto SL, Caplan JL, Hsueh YH, Kearns DB, Wu YS, Bais HP: Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol 2012, 160:1642-1661. 99. Eichmann R, Schafer P: Growth versus immunity — a redirection of the cell cycle? Curr Opin Plant Biol 2015, 26: 106-112. 100. Slovak R, Ogura T, Satbhai SB, Ristova D, Busch W: Genetic control of root growth: from genes to networks. Ann Bot 2015. 101. Satbhai SB, Ristova D, Busch W: Underground tuning: quantitative regulation of root growth. J Exp Bot 2015, 66: 1099-1112. 102. Meijon M, Satbhai SB, Tsuchimatsu T, Busch W: Genome-wide association study using cellular traits identifies a new regulator of root development in Arabidopsis. Nat Genet 2014, 46:77-81. 103. Busch W, Moore BT, Martsberger B, Mace DL, Twigg RW, Jung J, Pruteanu-Malinici I, Kennedy SJ, Fricke GK, Clark RL et al.: A microfluidic device and computational platform for highthroughput live imaging of gene expression. Nat Methods 2012, 9:1101-1106. 104. Slovak R, Goschl C, Su X, Shimotani K, Shiina T, Busch W: A scalable open-source pipeline for large-scale root phenotyping of Arabidopsis. Plant Cell 2014, 26:2390-2403. 105. Rellan-Alvarez R, Lobet G, Lindner H, Pradier PL, Sebastian J, Yee MC, Geng Y, Trontin C, LaRue T, Schrager-Lavelle A et al.: GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems. Elife 2015:4.

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