Breakout — lateral root emergence in Arabidopsis thaliana

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ScienceDirect Breakout — lateral root emergence in Arabidopsis thaliana

Dorothee Stoeckle1,3, Martha Thellmann1,3 and Joop EM Vermeer1,2 Lateral roots are determinants of plant root system architecture. Besides providing anchorage, they are a plant’s means to explore the soil environment for water and nutrients. Lateral roots form post-embryonically and initiate deep within the root. On its way to the surface, the newly formed organ needs to grow through three overlying cell layers; the endodermis, cortex and epidermis. A picture is emerging that a tight integration of chemical and mechanical signalling between the lateral root and the surrounding tissue is essential for proper organogenesis. Here we review the latest progress made towards our understanding of the fascinating biology underlying lateral root emergence in Arabidopsis.

Addresses 1 Department of Plant and Microbial Biology, University of Zurich, Switzerland 2 Cell Biology and Developmental Biology, Wageningen University, The Netherlands Corresponding author: Vermeer, Joop EM ([email protected]. ch) 3 Equal contribution. Current Opinion in Plant Biology 2018, 41:67–72 This review comes from a themed issue on Growth and development

endodermis, the cortex, and the epidermis. LRP growth is classified into 8 stages (Figure 1). Stages I–IV take place before growth through the endodermis, whereas stages V–VIII occur after this resistant cell layer has been crossed [1]. LR emergence is often considered as the step in which the LR breaches the surface of the root. However, this process initiates during the formative cell divisions leading to a stage I LRP and is therefore much more complex than it might appear. Recent findings suggest that LR emergence is a biphasic process in which the endodermis plays a crucial role. Endodermal feedback is required for the execution of the formative divisions and for the growth of the LRP through this persistent cell layer [2,3]. As LR formation depends on differential growth of the XPP, and since plant cells are interconnected through their cell walls, the growing LRP needs to deal with the mechanical constraints imposed by surrounding tissues. Therefore, LR formation strongly depends on the integration of both chemical and mechanical cues. Here we focus on the complexity of LR emergence and the regulatory and mechanistic processes behind it. The latest findings on processes such as LR priming, FC specification and initiation have been discussed comprehensively in recently published reviews [4,5].

Edited by Gwyneth Ingram and Ari Pekka Ma¨ho¨nen For a complete overview see the Issue and the Editorial

Lateral root growth promotion by auxin

Available online 29th September 2017

Auxin is required for both initiation and the development of LRs. Auxin signalling involves a set of core components: indole-3-acetic acid (IAA), binds to a co-receptor complex containing one of six TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALLING F-BOX (TIR1/AFB) receptor proteins and one of 29 transcriptional repressors called Aux/IAAs. Interestingly, these composite auxin receptors exhibit different levels of sensitivity [6,7]. To execute auxin signalling, proteasome-mediated degradation of the respective Aux/IAA results in the de-repression of its cognate AUXIN RESPONSE FACTOR (ARF), a family of 22 transcription factors [8]. The interaction of specific Aux/IAAs with certain ARFs leads to the formation of different signalling modules thereby generating specificity. Together with the extensive auxin fluxes throughout the plant and within tissues, this enables the establishment of different gene expression patterns resulting in many developmental outputs. These highly polarised transport processes are regulated by auxin influx and efflux carriers of the AUXIN RESISTANT 1 (AUX1)/LIKE AUX1 (LAX) and PIN-FORMED (PIN) families, respectively [9].

http://dx.doi.org/10.1016/j.pbi.2017.09.005 1369-5266/ã 2017 Elsevier Ltd. All rights reserved.

Introduction Plant cells control growth by creating and channeling forces in a very elegant and tightly-regulated manner. Shape is maintained by the interplay of turgor pressure and cell wall stiffness. Since plant cells are interconnected through their cell walls, no sliding or movement can normally occur. Therefore, any organogenesis, such as lateral root (LR) formation, needs to be a highly coordinated and regulated process. Unlike the primary root, lateral roots are formed post-embryonically. They initiate from specialised xylem pole pericycle (XPP) cells — the designated founder cells (FCs), deep within existing roots. On their way out, lateral root primordia (LRP) must traverse three cell layers: the neighbouring www.sciencedirect.com

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68 Growth and development

Figure 1

(a)

founder cells (FCs)

endodermis

cortex

epidermis

IAA28

SLR/IAA14

BDL/IAA12

ARF7

ARF7/19

ARF5/MP

FC

(b)

lateral root primordium (LRP)

I

II

III

IV

V

VI

VII

VIII side

SHY2/IAA3

SLR/IAA14

ARF7/?

ARF7/19

1a

1b

pGATA23::3mCherry-SYP122/pCASP1::Citrine-SYP122

LAX3

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auxin flow

VIII top

2b

VIII side pUBQ10::EYFP-NPSN12 (W131Y)

VIII top

Current Opinion in Plant Biology

Lateral root emergence in Arabidopsis thaliana. (a) Founder cells (FC, orange) are specified in the XPP and pass through eight developmental stages to emerge at the surface of the root. Stages I–IV take place before the endodermis is traversed (indicated by magenta dotted line) and stages V–VIII take place after the endodermis has been crossed. The LRP is indicated in yellow, the endodermis in cyan and the cortex and epidermis in different shades of magenta. LAX3 induction in overlying cortex cells is indicated by blue outlining of the cell wall. Auxin flows are indicated by red arrows. Dashed outlines of cortex and epidermis reflect their displacement into different planes of view with respect to the LRP; compare stage VIII side and top views. Different Aux/IAA-ARF modules regulate different phases of LR emergence. Whereas most modules are well characterised, little is known about the ARFs regulating endodermal responses. (b) Accommodating responses of the endodermis during growth of the LRP through this cell layer (1a, 1b) are completely different from the responses in the cortex and epidermis (2a, 2b). LRP is labelled in yellow in 1a, ( pGATA23::3mCherry-SYP122), whereas the endodermis plasma membrane is labelled cyan in 1a/b, ( pCASP1::mCitrine-SYP122) and all plasma membrane are labelled magenta in 2a/b, ( pUBQ10::EYFP-NPSN12). Scale bars: 10 mm.

Several Aux/IAA-ARF modules have been implicated in driving LR formation. The IAA28 — ARF5/6/7/19 module is specific for priming and founder cell specification [10–12]. For LR initiation and patterning the repression of ARF5 by BODENLOS (BDL)/IAA12 and ARF7/19 by SOLITARY ROOT (SLR)/IAA14 needs to be lifted to activate the cell cycle to form a LRP [13–16]. In addition, the SLR/ARF7/19 module acts in the cortex and epidermis overlying the LRP where it regulates cell wall remodelling (CWR) genes facilitating LR emergence [17]. It was shown that accommodating responses by the endodermis are crucial for LR development and emergence. These responses appear to be regulated by SHORT HYPOCOTYL 2 (SHY2)/IAA3. It is not known yet which ARFs are functioning in this module, although it has been Current Opinion in Plant Biology 2018, 41:67–72

shown that SHY2 can interact with several ARFs including ARF7 and ARF19 [2,18,19]. Interestingly, recent work demonstrated a non-canonical auxin sensing mechanism for the ARF3/ETTIN (ETT) protein, which lacks the PB1 domain responsible for ARF–Aux/IAA interaction [20,21]. Loss-of-function and auxin-insensitive mutants of ETT have an enhanced number of emerged LRs suggesting that IAA directly regulates ETT activity and normally negatively regulates LR development [21]. Downstream of ARF7 (and potentially other ARFs), several members of the LATERAL ORGAN BOUNDARIES DOMAIN/ASYMMETRIC LEAVES2-LIKE www.sciencedirect.com

Breakout – lateral root emergence in Arabidopsis thaliana Stoeckle, Thellmann and Vermeer 69

(LBD/ASL) protein family are also required for LR development. LBD16 is a primary target of ARF7 and is required for nuclear migration and the first asymmetrical division [13]. LBD18/33 and LBD29 promote cell cycle regulation in LRP [22,23], but are also expressed in cell layers overlaying the primordia. LBD18 has been shown to function during LR emergence through direct regulation of the CWR enzyme-encoding gene EXPANSIN14 (EXP14) and EXP17. LBD18 expression is positively regulated by LAX3, which was already known to regulate the expression of several CWR enzyme-encoding genes to facilitate emergence [17,24]. Porco et al. have shown that besides expression in the LRP, LBD29 is also induced in endodermis and cortex cells overlying the LRP. Neither LAX3 nor its targets could be induced in the lbd29-1 mutant. Likewise, LBD29 directly binds the LAX3 promoter and ectopic expression of LBD29 results in enhanced expression of LAX3 in the cortex in all parts of the root [25]. The LBD29 promoter is itself a direct target of ARF7 [26].

Lateral root growth restriction via cytokinin Cytokinin (CK) antagonizes auxin signalling by promoting the degradation of PIN proteins [27] and interfering with polar auxin transport. Overproduction of CK inhibits LR initiation while degradation of CK results in an increased number of LRs [28,29]. The use of a CK signalling output reporter revealed an enhanced response in the XPP cells between forming LRP, indicating a role in LR spacing through suppression of initiation [30]. Little is known about roles of CK during LR emergence. However, a recent report identifying the family of PURIN PERMEASE PROTEINs (PUPs) as CK transporters predicted them to control the spatiotemporal landscape of CK signalling. Reducing the transcript levels of PUP14 led to ectopic expression of the CK reporter TCSn1::GFP and seedlings displayed shorter roots and no LRs suggesting a role for PUP14 in LR formation [31]. Since the Arabidopsis PUP family has 23 members [31] it will be interesting to test whether some PUPs are expressed in cells overlying the LRP thereby modifying CK signalling and thus LR emergence.

cell division pattern and organ growth, LRP shape was still normal [34]. Using 4D imaging light-sheet fluorescence microscopy (LSFM), von Wangenheim et al., recently revealed how the LRP develops and emerges in a very regulated manner. They showed that the LRP takes more time to transit the endodermis than the other cell layers despite the fact that the cells of the LRP showed the same cell division rate when passing the cortex and the epidermis [35,36]. The presence of a localized primary cell wall modification, the Casparian strip (CS), which acts as an apoplastic diffusion barrier, may turn the endodermis into a tough hurdle to cross. As the CS is made up out of lignin it is both non-extendable and resistant to chemical degradation, rendering the endodermis a particular tenacious cell layer [37].

Shape change and volume loss in the endodermis Using live cell imaging, it was shown that early during LR formation endodermal cells need to change shape and lose volume to accommodate the expansion of the LRP. This feedback is already required to enable formative cell divisions leading to a stage I LRP. As the LRP develops, endodermal cells undergo a drastic loss of volume and become flattened to a point where the upper and lower plasma membrane fuse and retract to provide space for the growing LRP. In addition, Arabidopsis is able to locally modify the CS to allow for a regulated growth of the LRP through the endodermis [2]. Remarkably, programmed cell death does not seem to be a major contributor to this process as the endodermal cells remain alive during this drastic loss of cell volume (Fig. 1) [2,35]. Auxin signalling seems to be the main regulator of the endodermal accommodating responses. The Aux/IAA SHY2 is specifically induced in the endodermal cells overlying the LRP. Blocking these responses by expressing the SHY2 gain-of-function allele shy2-2 specifically in differentiating endodermal cells ( pCASP1::shy2-2), resulted in a complete block of LR formation. Treating these plants with auxin supported the biphasic nature of LR emergence: although auxin treatment could induce LR initiation, the LRP was still not able to grow through the endodermis as this layer remained turgid [2].

Integration of mechanical cues into lateral root growth

Hydrodynamics

The process of LR emergence also provides a fascinating system to study the interplay between chemical and mechanical signals. The LRP needs to overcome the mechanical constraints imposed by the overlying cell layers. Normally, mechanical forces restrict growth [32,33], but during LR formation surrounding cells need to accommodate growth of the newly formed organ. Lucas et al., showed that the mechanical properties of overlying cell layers, rather than intrinsic cell division patterns, shape the LRP. It was shown that in the aurora1 (aur1),aur2 double mutant, which displays a disrupted

The important role of cell volume regulation emphasises the importance of the regulation of water transport. Two different types of aquaporins facilitate LR emergence: Plasma membrane Intrinsic Proteins (PIPs) and Tonoplast Intrinsic Proteins (TIPs) [38,39]. Pe´ret et al., showed that ARF7-mediated regulation of the aquaporin PIP2;1 is important for LR emergence. Both the PIP2;1 loss-of-function and gain-of-function mutants show delayed emergence [38]. TIPs are expressed, depending on their isoform, in all root cell layers except the epidermis. The tip1;1,tip1;2,tip2;1 triple mutant displayed a

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delay in LR emergence. Whereas ectopic expression of PIP2;1 resulted in flattened LRP, this was not observed when the TIP isoforms were ectopically expressed [38,39]. Taken together, plasma membrane and tonoplast localized aquaporins seem to have distinct functions in LR emergence. The symplastic interconnectivity between cells is another factor involved in LR emergence. Modulation of symplastic connectivity through plasmodesmata has not only been shown to affect LR initiation and spacing, but also has been implicated in LR emergence. Overexpression of PLASMODESMATA CALLOSE BINDING PROTEIN1 (PDCB1) reduces LR emergence, whereas treatment with the glucose analogue 2-deoxy-D-glucose (DDG), which inhibits callose formation, results in enhanced LR emergence. However, the underlying mechanism(s) are not yet clear [40]. It will be important to elucidate the specific contributions of aquaporins and plasmodesmata in the regulation of hydrodynamics during LR emergence. Are they operating in the same pathway or do they have independent functions? Is the gating of symplastic connectivity a means of establishing differential turgor pressure between different cell layers?

Cell wall remodelling The importance of cell shrinkage and cell separation during LR emergence implies extensive CWR. In addition to the role of LAX3-dependent regulation of the expression of genes encoding CWR enzymes, other important regulators have been reported. Kumpf et al., showed that the leucine-rich repeat receptor-like kinases HAESA (HAE) and HAESA-LIKE2 (HSL2), together with their ligand INFLORESCENCE DEFICIENT IN ABSCISSION (IDA), regulate CWR in cell layers overlying LRP. Although initially identified as factors regulating floral abscission, mutation of these genes also leads to delayed LR emergence and the formation of LRP with flattened shapes [41]. Recently, Orman-Ligeza et al., reported that reactive oxygen species (ROS) generated by RESPIRATORY BURST OXIDASE HOMOLOGS (RBOHs) facilitate LR emergence by promoting CWR in overlying cell layers. They showed that genes encoding several RBOHs are induced in tissues overlying LRP, and that loss-of-function mutants show delayed LR emergence. Interestingly, they also demonstrated that H2O2 treatment can restore LR formation in mutants where auxin-mediated cell wall accommodation and remodelling in overlying cell layers is disrupted such as the aux1, lax3 and pCASP1::shy2-2 mutants [42]. After passing the endodermis the LRP have an ‘easy life’ on their way out. Although they also stay alive during LR emergence, overlying cortical and epidermal cells do not undergo noticeable volume loss, they are just pushed aside by the LRP after CWR enzymes have degraded their middle Current Opinion in Plant Biology 2018, 41:67–72

lamellae [2,41]. Interestingly, CWR enzymes induced in overlying cell layers do not seem to act on the LRP, which appears to be protected through the secretion of suberin-like compounds [43]. Additionally, tight spatiotemporal regulation of CWR enzyme expression should contribute ensuring localized activity.

Future challenges Although we have made major steps in understanding the complex biology underlying LR emergence in Arabidopsis, some questions still remain unanswered. Though it is clear that there is a complex interplay of chemical and mechanical signals during this process, it is remarkable how little we know about the role of the cytoskeleton in LR formation. As cell wall modification is important to facilitate LR formation, it will be important to map changes in cell wall composition during LR emergence [44]. With all the improved imaging methods and cell type-specific promoters, now is the right time to start filling in these blanks. As shown by von Wangenheim et al. [36] LSFM is a powerful approach to follow the complete process of LR formation from initiation to emergence at the root surface, under near physiological conditions. A major challenge will be to use 3D-segmentation to extract cell shapes and volumes during this process to start building 3D models that incorporate mechanical signals as well as the interplay between the LRP and the surrounding tissues on a cellular scale. A similar approach has been successfully used to gain important insights in the development of the shoot apical meristem [45]. Furthermore, it will be important that we can measure mechanical parameters in internal cell layers without affecting the integrity of the overlying tissues in order to infer models of LR emergence. The recently described fluorescence emission-Brillouin imaging approach seems very promising [46]. Arabidopsis has been, and still is, instrumental in gaining a better understanding of organogenesis. However, there is already quite a body of work on LR emergence in different (crop) species that has revealed clear differences compared to Arabidopsis LR development [47–51]. Due to vast technological improvements (i.e. genome editing, sequencing technologies) it is now feasible to look further than Arabidopsis to determine to what extent the mechanisms described for Arabidopsis are applicable across different species. Finally, it is also important to start imaging plants in their natural environment, to compare phenotypes observed on plates to those observed in the soil. To this end, recent advancements in X-ray microcomputed tomography and bioluminescence-based systems like the GLO-ROOT system will be important to get a more complete view of the biology underlying LR emergence [52,53]. www.sciencedirect.com

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39. Reinhardt H, Hachez C, Bienert MD, Beebo A, Swarup K, Voss U,  Bouhidel K, Frigerio L, Schjoerring JK, Bennett MJ et al.: Tonoplast aquaporins facilitate lateral root emergence. Plant Physiol 2016, 170:1640-1654. The authors show for the first time that TIP proteins have a function during LR formation. Interestingly, ectopic expression of TIPs does not result in similar phenotypes as ectopic expression of PIPs.

50. Peret B, Larrieu A, Bennett MJ: Lateral root emergence: a difficult birth. J Exp Bot 2009, 60:3637-3643. 51. Yu P, Gutjahr C, Li C, Hochholdinger F: Genetic control of lateral root formation in cereals. Trends Plant Sci 2016, 21:951-961.

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52. Mairhofer S, Sturrock CJ, Bennett MJ, Mooney SJ, Pridmore TP:  Extracting multiple interacting root systems using X-ray microcomputed tomography. Plant J 2015, 84:1034-1043. The authors report major improvements in analysing root systems in the soil using X-ray microcomputed tomography.

41. Kumpf RP, Shi CL, Larrieu A, Sto IM, Butenko MA, Peret B, Riiser ES, Bennett MJ, Aalen RB: Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proc Natl Acad Sci U S A 2013, 110:5235-5240.

53. 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.

Current Opinion in Plant Biology 2018, 41:67–72

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