Branching out in new directions: the control of root architecture by

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Branching out in new directions: the control of root architecture by lateral root formation

C. Nibau*, D. J. Gibbs* and J. C. CoatesSchool of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK

Contents

Summary 595

I. Background 595

II. Formation of lateral roots 596

III. Endogenous factors regulating the stages of lateral root development 597

IV. Plasticity: modification of lateral root development by the environment 603

V. Transcriptomic studies to identify potential new regulators of lateral root development 608

VI. Conclusions and future challenges 608

Acknowledgements 608

References 609

Author for correspondence:J. C. CoatesTel: +44 121 414 5478Fax: +44 121 414 5925Email: [email protected]

Received: 21 December 2007Accepted: 14 March 2008

Summary

Plant roots are required for the acquisition of water and nutrients, for responses toabiotic and biotic signals in the soil, and to anchor the plant in the ground. Controllingplant root architecture is a fundamental part of plant development and evolution,enabling a plant to respond to changing environmental conditions and allowing plantsto survive in different ecological niches. Variations in the size, shape and surface area ofplant root systems are brought about largely by variations in root branching. Muchis known about how root branching is controlled both by intracellular signalling pat-hays and by environmental signals. Here, we will review this knowledge, with particularemphasis on recent advances in the field that open new and exciting areas of research.

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© The Authors (2008). Journal compilation © New Phytologist (2008) doi: 10.1111/j.1469-8137.2008.02472.x

I. Background

A plant’s root system is the site of water and nutrient uptakefrom the soil, a sensor of abiotic and biotic stresses, and a

structural anchor to support the shoot. The root systemcommunicates with the shoot, and the shoot in turn sendssignals to the roots. A plant root system initially consists of aprimary root (PR) formed during embryogenesis that hasdividing cells in a meristem at its tip. As the seedling develops,certain other cells within the PR acquire the capability to*These authors contributed equally to this work.

Key words: abiotic stress, biotic stress, lateral root development, nutrients, plant hormones, root system architecture, transcriptomics.

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divide, eventually forming new roots, called lateral roots (LRs)(Fig. 1a). These branch out from the PR, greatly increasingthe total surface area and mechanical strength of the rootsystem and allow the plant to explore the soil environment.Ultimately, millions of higher-order root branches can form,resulting in hundreds of miles of root system in a small areaof soil (Dittmer, 1937). New roots, called adventitious roots(AR), can also be formed postembryonically at the shoot–rootjunction, optimizing the exploration of the upper soil layers(Fig. 1a). In cereals such as rice and maize, root structurebecomes more complex, with the formation of additionalshoot-borne and postembryonic roots, which in turn undergohigher-order branching (Hochholdinger et al., 2004; Hoch-holdinger & Zimmermann, 2008; Fig. 1b).

The root system architecture (RSA) of plants varies hugelybetween species and also shows extensive natural variationwithin species, reflecting the plethora of environments inwhich plants can grow (Cannon, 1949; Loudet et al., 2005;Osmont et al., 2007). Root system architecture manipulationis instrumental in the domestication and breeding of cropplants, because using water and nutrients from the soil in themost efficient manner affects a plant’s ability to survive instressful or poor soils. Changes in RSA can therefore havehuge impacts on the final yield of a crop (reviewed in deDorlodot et al., 2007). Of the factors that control total RSA,LR formation and growth is one of the most important.

Many of the hormonal and environmental signals affectingLR development also affect other components that have abearing on RSA and the overall root surface area, namely, root

hair development, primary root (PR) growth and AR formation.However, an extensive analysis of how these structures arecontrolled is outside the scope of the present review and thereader is referred to several other excellent reviews (Dolan &Costa, 2001; Carol & Dolan, 2002; Scheres et al., 2002; Casson& Lindsey, 2003; Hochholdinger et al., 2004; Samaj et al., 2004;Serna, 2005; Scheres, 2007). Moreover, colonization of certainplant roots by symbiotic bacteria or fungi leads to the formationof modified LRs (root nodules, mycorrhizas or proteoid roots)that carry out specialized functions such as nutrient acquisition(Oldroyd & Downie, 2004, 2006; Autran et al., 2006).

In addition to signals that regulate many components ofRSA (and sometimes also shoot development), there ismounting evidence that some signalling networks are specificfor LR formation (Rogg et al., 2001; Hochholdinger et al.,2004; Loudet et al., 2005; Coates et al., 2006), potentiallyhighlighting novel strategies for manipulating root branchingin crop plants.

Because of the major contribution they play in the controlof RSA, this review focuses on LRs: how they arise and develop.It will pay particular attention to recent molecular and ‘omic’developments that highlight the huge variety of genes,proteins and mechanisms that interact together to coordinatea process so central to plant development and survival.

II. Formation of lateral roots

In flowering plants and gymnosperms, LRs initiate from aspecialized cell layer in the PR called the pericycle. Thepericycle is the outermost cell layer of the vascular cylinderand consists of two distinct cell types corresponding to theunderlying vasculature (Dubrovsky & Rost, 2005; Parizotet al., 2008; Fig. 2a,b). In Arabidopsis and most other dicots,LRs are formed only from pericycle cells overlying thedeveloping xylem tissue (the xylem pole pericycle) (Fig 2b). Inother species, particularly cereals such as maize, rice and wheat,LRs arise specifically from the phloem pole pericycle, withadditional contributions from the endodermis (De Smet et al.,2006a; Hochholdinger & Zimmermann, 2008; Fig. 2b).

Insights into the evolution of multicellular, branched rootsystems come from ‘ancient’ plants. In a vascular nonseedplant, the fern Ceratopteris, LRs arise from the endodermisand may be regulated differently from those in floweringplants (Hou et al., 2004). The bryophyte moss Physcomitrellapatens revealed a very ancient mechanism controlling thedevelopment of tissues with a rooting function (Menand et al.,2007). Physcomitrella possesses putative homologues of knownArabidopsis LR regulators, many of which have no assignedfunction (e.g. Axtell et al., 2007; Rensing et al., 2008).

Lateral root formation consists of four key stages: (i)stimulation and dedifferentiation of pericycle founder cells;(ii) cell cycle re-entry and asymmetric cell divisions to give riseto a lateral root primordium (LRP); (iii) LRP emergencethrough the outer layers of the PR via cell expansion; and (iv)

Fig. 1 Components of the root system. (a) A typical dicot (e.g. Arabidopsis) seedling root system, consisting of a primary root (PR) originating from the embryo, lateral roots (LR) branching out from the PR during seedling development, and root hairs (RH) that originate from PR epidermal (Epi) cells (shown at higher magnification to the right (inset)). Ultimately, the LRs will undergo higher-order branching to form secondary and tertiary LRs. Adventitious roots (AR) form at the shoot–root junction. (b) A typical cereal (e.g. rice, maize) seedling root system consisting of a primary root (PR) originating from the embryo, seminal roots (SR) that originate postembryonically close to the top of the primary root, and crown roots (CR) that originate from the stem. PR, SR and CR all form LR and undergo higher-order branching.

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activation of the LR meristem that recapitulates PR growth(Celenza et al., 1995; Cheng et al., 1995; Laskowski et al.,1995; Malamy & Benfey, 1997).

III. Endogenous factors regulating the stages of lateral root development

Underpinning each stage of LR development is the hormoneauxin (Casimiro et al., 2003; Woodward & Bartel, 2005;Figs 3a–d and 4a–d). Comprehensive studies using a LR-

inducible system revealed that over 10% of the Arabidopsisseedling root transcriptome was affected by treatment withauxin (Himanen et al., 2002; Vanneste et al., 2005).

Auxin maxima appear at LR initiation sites and also laterduring emergence and elongation (see section III.1). Auxin‘hot spots’ within the root arise as a result of the regulatedpositioning of auxin transporters within cells, in a processconserved between lateral organ formation in the root and inthe shoot (Benkova et al., 2003). Interestingly, auxin signallingregulates the differential positioning of auxin efflux carriers

Fig. 2 Root anatomy. (a) Longitudinal section through an Arabidopsis primary root tip, showing the different cell types. LRC, lateral root cap (which is absent further up the root); Epi, epidermis (which is the outermost layer of the root above the root tip); Co, cortex; En, endodermis; P, pericycle; Vasc, vasculature (xylem and phloem); QC, quiescent centre (maintains the neighbouring stem cell population). (b) Transverse section through an Arabidopsis primary root. Epi, epidermis; RH, root hair; Co, cortex; En, endodermis; P, pericycle; XPP, xylem pole pericycle (the pericycle cells adjacent to the xylem tissue, from which lateral roots arise); Xy, xylem; Ph, phloem. In monocots, lateral roots arise from the phloem pole pericycle.

Fig. 3 Aspects of auxin signalling during lateral root (LR) development. (a) A pulse of auxin (light grey) in the basal meristem (BM) primes a pericycle cell (dark grey) to become competent to form a lateral root initial cell. (b) Cells (white) leaving the basal meristem between cyclical auxin maxima are not specified to become LR initials. (c) The first primed pericycle cell arrives at a point where it can initiate LR development; meanwhile another pericycle cell (dark grey) is primed in the basal meristem by the subsequent auxin pulse. (d) Lateral root initiation begins with auxin-induced IAA14 degradation. This allows activation of the ARF7 and ARF19 transcription factors, which activate expression of LBD/ASL genes. LBD/ASL proteins in turn activate cell cycle genes and cell patterning genes, enabling formation of a new lateral root primordium (LRP). Auxin also activates transcription of NAC1 to stimulate LR initiation, and at the same time induces expression of two ubiquitin ligases, CEGUENDO and SINAT5, which feed back to attenuate the auxin response.

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and, consequently, the direction of auxin flow (Sauer et al.,2006). This effect is mediated by the activity of VPS29, amembrane-trafficking component that is involved in therecycling of cargo molecules. Together with other proteins,VPS29 mediates the dynamic arrangement of auxin effluxcarriers in response to auxin (Jaillais et al., 2007). The regulatedinterplay between auxin transport and signalling is critical forall stages of LR development, and many of the signals regulatingRSA impinge upon this pathway.

Many Arabidopsis and cereal mutants affecting auxin pro-duction, transport and metabolism have LR defects: theirinvolvement in LR formation has been described extensivelyelsewhere (Casimiro et al., 2003; Woodward & Bartel, 2005;Fukaki et al., 2007). Lack of detailed characterization of manyof these mutants prevents identification of the particular stageof LR development at which they act (De Smet et al., 2006a).Exhaustive description of all the proteins involved inauxin-dependent lateral organ formation is beyond the scopeof this review and the reader is directed to recent reviews inthis area (De Smet et al., 2006a; Teale et al., 2006; De Smet& Jurgens, 2007).

Other hormone pathways are also involved in the regulationof LR formation, and recent research provides new insightinto these pathways. Below we will outline how plant hor-mones, with particular emphasis on auxin, interact with variouscellular processes to control each stage of LR development.

1. Lateral root initiation – stimulation of cell cycle proliferation in the pericycle

In Arabidopsis, the xylem pole pericycle cells, from which LRsarise, are smaller than other pericycle cells, indicating

differential cell cycle regulation between pericycle cell types.Normally, not all xylem pole pericycle cells form LRP,indicating that multiple levels of control occur in these cells(Beeckman et al., 2001). However, exogenous application ofauxin can activate the whole pericycle to form LRPs, whereasthe application of auxin transport inhibitors blocks LRformation without loss of pericycle identity (Casimiro et al.,2001; Himanen et al., 2002). Therefore, all the cells withinthe pericycle retain the ability to form LRs but only some ofthem do so. It is thus suggested that the coordinated action ofauxin transport and signalling, cell cycle regulators and novelroot-specific proteins is necessary for LR initiation to occur.

Lateral root initiation requires auxin and regulated proteindegradation Auxin signalling during LR initiation is closelycoupled with regulated protein degradation (Fig. 3d). Proteinsare targeted to the cellular degradation machinery, theproteasome, by the addition of a chain of ubiquitin monomers.The process requires a ubiquitin-activating enzyme (E1), aubiquitin-conjugating enzyme (E2) and a ubiquitin-proteinligase (E3), which transfers ubiquitin from the E2 to thetarget (Petroski & Deshaies, 2005). Some E3 ubiquitin ligasesconsist of multiprotein complexes, and SKP1-CULLIN1-F-box(SCF) E3 ligases contain F-box protein subunits that conferspecificity, binding to particular target proteins.

Auxin receptors are a family of F-box-containing proteinsknown as TIR1 and AFB1–3 (Dharmasiri et al., 2005a,b;Kepinski & Leyser, 2005). It is thus not surprising thatmutants in components of the SCF complex and its associatedproteins have altered LR phenotypes (Gray et al., 1999; Hell-mann et al., 2003; Bostick et al., 2004; Chuang et al., 2004;Woodward et al., 2007).

Fig. 4 Lateral root development in Arabidopsis shown in longitudinal section. P, pericycle; En, endodermis; Co, cortex; Epi, epidermis. (a) Early initiation – a founder xylem pole pericycle cell (dark grey) undergoes initial anticlinal cell divisions (perpendicular to the surface of the root). (b) Periclinal cell divisions (parallel to the surface of the root) begin and the lateral root primordium (LRP) begins to grow. (c) The LRP undergoes further organized cell divisions and begins to emerge through the outer cell layers of the primary root, resulting in cell separation (asterisks). (d) The new lateral root is fully emerged and its new meristem is activated (dark grey star). It will continue to grow and elongate. At each stage, the effect of various key plant hormones is indicated. ABA, abscisic acid; BR, brassinosteroids.

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Auxin binding to TIR1/AFBs allows them to interact withAUX/IAA proteins and target them for degradation. AUX/IAAproteins are transcriptional repressors that dimerize withauxin response factor (ARF) transcription factors, preventingthe latter from binding to promoter elements in auxin-responsive genes. Thus, auxin-induced degradation of AUX/IAAs enables ARFs to activate auxin-responsive transcription(Gray et al., 2001; Dharmasiri et al., 2005a,b; Kepinski &Leyser, 2005). AUX/IAAs and ARFs exist as large, functionallyredundant protein families (Okushima et al., 2005; Overvoordeet al., 2005).

One of the most important AUX/IAA proteins for LRinitiation is SLR1/IAA14. As a result of the stabilizationof IAA14, a gain-of-function slr1 mutant does not form LRs(Fukaki et al., 2002). In wild-type plants, auxin triggersthe degradation of IAA14, enabling ARF7 and ARF19 toactivate transcription of LATERAL ORGAN BOUNDARIESDOMAIN/ASYMMETRIC LEAVES LIKE (LBD/ASL) genes(Fukaki et al., 2005; Okushima et al., 2007; and Fig. 3d).LBD/ASL proteins, in turn, activate the transcription of cellproliferation and patterning genes (Okushima et al., 2007).In maize and rice, LBD genes regulate shoot-borne rootformation rather than LRs (Taramino et al., 2007; Hoch-holdinger & Zimmermann, 2008). ARF7 also interacts witha MYB transcription factor that provides a link among auxin,LR initiation and environmental responses (Shin et al., 2007;and section IV.4).

Comparison of the auxin-induced transcriptomes ofwild-type and slr1 roots identified 913 specific ‘LR initiation’genes that function downstream of the auxin/slr1 signallingpathway. Many of these are cell cycle-associated genes or celldivision-associated genes, and genes involved in auxin signalling,transport or metabolism. Other over-represented functionalcategories include macromolecular biosynthesis, ribosomebiogenesis and DNA synthesis (Vanneste et al., 2005).

IAA28 is also important for LR initiation. The gain-of-function mutant iaa28 forms fewer LRs than the wild type:IAA28 is degraded by auxin and represses auxin-inducedLR-formation genes. However, IAA28 mRNA levels arerepressed by auxin, indicating a complex regulation of IAA28during auxin signalling (Rogg et al., 2001; Dreher et al.,2006). The iaa28 mutant is also resistant to exogenous cyto-kinins and ethylene, suggesting an integration point for otherhormone pathways.

The VIER F-BOX PROTEINE (VFB) F-box proteinsare also important for LR formation in Arabidopsis. Mutantsdeficient in VFB function have reduced LR formation. Micro-array analysis demonstrated that loss of VFB function leads toaltered expression of both auxin-responsive genes and cellwall-remodelling genes (Schwager et al., 2007). Despite this,vfb mutant plants maintain full sensitivity to exogenouslyapplied auxin. VFBs may regulate auxin-induced gene exp-ression, and consequently LR formation, by a pathwayindependent of the auxin receptor TIR1 (Schwager et al.,

2007). It will be important to determine whether IAA14/SLR1 stability or cell cycle gene expression is affected in vfbmutants.

The NAC1 transcription factor promotes LR initiation(Xie et al., 2000) and may bind auxin-responsive promotersto transmit the auxin signal (Fig. 3d). Interestingly, NAC1overexpression can rescue the reduced LR phenotype of tir1auxin receptor mutants. NAC1 is tightly regulated: NAC1expression is induced within 30 min of auxin application,suggesting that NAC1 may be an early auxin-responsive gene.Auxin also induces the expression (albeit more slowly) ofSINAT5, a RING-finger ubiquitin E3 ligase (Fig. 3d). SINAT5promotes NAC1 ubiquitination and subsequent degradation(Xie et al., 2002). It will be interesting to determine if auxinbinds directly to SINAT5 in the SINAT5–NAC1 complex.

Yet another ubiquitin ligase involved in LR initiation isXBAT32 (Nodzon et al., 2004). XBAT32 is a RING-fingerprotein highly expressed in the vascular system close to sites ofLR initiation. Plants lacking XBAT32 develop fewer LRs thanwild-type plants and have reduced cell division in the pericycle.XBAT32 may be involved in auxin transport: loss of XBAT32may lead to suboptimal auxin levels for LR initiation (Nodzonet al., 2004).

As only certain pericycle cells usually give rise to LRs, it iscrucial that auxin signals are tightly regulated. Interestingly,auxin stimulates the transcription of ubiquitin ligases thatrepress auxin signals, providing an elegant feedback mechanismto maintain auxin sensitivity in the pericycle. The F-boxprotein CEGENDUO (CEG) is a negative regulator of LRformation whose transcription is induced by auxin (Donget al., 2006; and Fig. 3d). Further studies are needed to clarifyits role LR initiation.

It is thus clear that the action of auxin during LR initiationdepends heavily on the ubiquitin-proteasome pathway, bothto transduce signals by degrading repressors and also to resetthe system by destroying activators when they are no longerneeded. Protein degradation allows for rapid changes inresponse to the ever-changing environment, as well as provid-ing fine-tuning to sustained signals.

Which pericycle cells? Questions remain about where, whenand which pericycle cells are primed to become LR initiationsites. In the last year, this problem has been addressed by newmolecular genetic and mathematical modelling studies.

De Smet et al. (2007) showed that the position of ArabidopsisLR formation is determined in a region at the transition betweenthe meristem and the elongation zone, called the basal meristem(Fig. 3a–c). Lateral roots occurred in a regularly spaced alternatingleft–right pattern correlating with gravity-induced root waving.Both responses are dependent on the auxin influx transporter,AUX1. Furthermore, auxin responsiveness at the basal meristemoscillates in a periodic manner, correlating with the timing ofLR formation. This, together with the observation of a lateralgradient of auxin responsiveness with a maximum in protoxylem

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cells, led the authors to suggest that auxin accumulationalone is sufficient for the priming of founder cells (De Smetet al., 2007). Consequently, one can suggest that all the otherfactors involved in LR formation will act downstream of theauxin signal. However, several factors have been suggested toregulate LR formation independently of auxin (see sectionIII.1 ‘Hormone-independent signalling pathways that regulatelateral root initiation’). Targeted manipulation of these genesin pericycle cells in the basal meristem is necessary to clarifythis conundrum. In addition, it is well known that environ-mental factors can tap into the LR developmental programand alter root architecture in regions outside the basal meristem(see section IV).

Support for the co-regulation of LR formation and gravi-tropism came from a mathematical model suggesting thatgravistimulation concentrates auxin at a certain point in theroot, allowing the auxin threshold necessary for LR formationto be reached. Lateral root initiation would, in turn, consumethe auxin pool in that area, preventing new LR initiation untilthe pool had been refilled: this would be accelerated by a newgravistimulation (Lucas et al., 2007). Two main ideas cameout of this study: first, there is an endogenous mechanismregulating the periodicity of LR formation, revealed by theexistence of a minimum and maximum time between twosuccessive LR initiations. Second, this endogenous system issensitive to external cues such as gravity (Lucas et al., 2007).This would provide increased plasticity for the root system toadapt to new soil conditions.

Interestingly, the developmental window for LR initiationin Arabidopsis displays natural variation between accessions(Dubrovsky et al., 2006), which may indicate adaptation ofthe system to different environmental niches. In addition,LRP initiation and emergence are separable processes, againproviding greater plasticity to the root system (Dubrovskyet al., 2006). The mathematical model used by Lucas et al.(2007) suggests that LR formation in gravistimulated areasmay also optimize soil exploration. It will be interesting todetermine if biotic and abiotic factors that alter RSA also havean effect on gravitropism-stimulated LR formation.

It is important to move this type of research beyondArabidopsis to agriculturally relevant plants, especially as themechanisms at work in crop plants may differ from thosein Arabidopsis. In many grasses, LRs initiate in phloem polepericycle cells and, because of varying root organization andgrowth rates, the timing and spacing of LR initiation is alsodifferent (Dubrovsky et al., 2006; Dembinsky et al., 2007).

Interplay between the cell cycle and auxin signalling It isgenerally accepted that pericycle cells are arrested in the G1phase of the cell cycle. Those pericycle cells that will give riseto a LR proceed through S phase and arrest in G2. Lateralroot-inducing signals stimulate these cells to undergoproliferative cell divisions (Beeckman et al., 2001). Cell cyclere-entry requires changes in chromatin structure, increasing

the proportion of active chromatin in the genome (DeVeylder et al., 2007). Indeed, a chromatin remodelling factormutant has perturbed LR initiation (Fukaki et al., 2006). Cellcycle progression from G1 to S requires the activity of theretinoblastoma (RB)-E2F pathway (del Pozo et al., 2006; DeVeylder et al., 2007). Progression from G2 to M is regulatedby the opposing activity of B-type cyclin-dependent kinases(CDKs) and CDK inhibitor proteins (KRPs) (Wang et al.,1997; De Veylder et al., 2001; Verkest et al., 2005). Many cellcycle components are transcriptionally regulated by auxin(Himanen et al., 2002; Vanneste et al., 2005). Another levelof regulation involves cell cycle protein degradation (Verkestet al., 2005; del Pozo et al., 2006).

In tomato, nitric oxide is required in the early stages of LRformation to regulate the expression of cell cycle genes, down-stream of the auxin signal (Correa-Aragunde et al., 2006).Nitric oxide is also induced in Arabidopsis LRP by the auxin,indole-3-butyric acid (Kolbert et al., 2007).

Despite the importance of the cell cycle in LR initiation,increasing the mitotic index in roots or forcing excessive celldivisions in the pericycle does not stimulate LR initiation ormorphogenesis (Vanneste et al., 2005; Wang et al., 2006).Thus, pericycle cell divisions can be uncoupled from LRPformation, and LR initiation seems to require the simultaneousactivation of cell cycle and cell fate genes triggered by auxin-induced degradation of the SLR/IAA14 protein (Vannesteet al., 2005). Conversely, although cell division and LRmorphogenesis are both controlled by auxin signalling, theprocesses are regulated independently, as shown by tomatodiageotropica (dgt) mutants that have a number of auxin-relatedphenotypes (including a lack of LRs) but have normal rootcell identities and patterning. dgt mutant pericycle cells maintaintheir full proliferative capacity, but no LRs are formed, evenin the presence of exogenous auxin, which instead stimulatesfurther pericycle divisions to form multiple cell layers(Ivanchenko et al., 2006). A similar mechanism operates inArabidopsis, as demonstrated by the wol mutant, which formsvery few LRs even in the presence of auxin (Parizot et al.,2008). Close analysis of the pericycle cells in the wol mutantshowed that they express pericycle protoxylem markers andare able to divide in response to auxin but no LRPs are formed(Parizot et al., 2008). This again shows that cell cycle activationis not sufficient for LR initiation to occur.

Heterotrimeric G-proteins may integrate auxin signalling andcell cycle inputs during root branching as well as other develop-mental processes (Ullah et al., 2001, 2003; Chen et al., 2006b;Trusov et al., 2007). Mutations in the β or γ G-proteinsubunits show increased cell division and increased LR forma-tion, and the normal function of Gβ and Gγ may be to attenuateauxin signalling (Ullah et al., 2003; Trusov et al., 2007).

Other hormones affecting LR development In addition toauxin, other hormone signals are important for LR initia-tion (Fig. 4a–d). Traditionally, cytokinin is thought to act

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antagonistically to auxin in many developmental processes:indeed, cytokinin is a negative regulator of LR formation inmany plant species, including Arabidopsis, Medicago, tobaccoand rice (Werner et al., 2003; Rani Debi et al., 2005;Gonzalez-Rizzo et al., 2006; Li et al., 2006b; Laplaze et al.,2007). Plants with decreased cytokinin content have increasedLR numbers (Werner et al., 2001, 2003; To et al., 2004;Mason et al., 2005; Gonzalez-Rizzo et al., 2006; Riefler et al.,2006), whereas exogenous cytokinin inhibits LR initiation bypreventing pericycle cell cycle re-entry (Li et al., 2006b). Anelegant study by Laplaze et al. (2007) showed that exogenouscytokinin disrupts both LR initiation and the organization ofcell divisions within developing LRPs: these defects cannot berescued by auxin. Targeted expression of cytokinin biosyntheticand catabolic enzymes in specific cell types demonstrated thatcytokinin activity is required very early in the LR formationprocess (Laplaze et al., 2007). Importantly, disrupting cytokininsignalling in xylem pole pericycle cells leads to perturbationof the auxin maximum in developing LRPs as a result of thereduced expression of PIN auxin transporter genes andmislocalization of PIN proteins (Laplaze et al., 2007).

Both ethylene and brassinosteroids affect LR formation viaan auxin-dependent pathway (Bao et al., 2004; Stepanovaet al., 2005). In rice, a casein kinase 1 gene, OsCKI, is upregu-lated by both brassinosteroid and abscisic acid (ABA) andpromotes lateral and AR formation as well as cell elongation.OsCKI may affect LR development by regulating endogenousauxin levels (Liu et al., 2003). Transcriptomic analysis ofOsCKI-deficient plants revealed alteration of several signalling,developmental, transcriptional and metabolic genes (Liuet al., 2003).

Unequivocal evidence for a role of ABA in LR initiation isnot available. However, the ABA-insensitive mutant abi3shows decreased sensitivity to auxin-induced LR initiation(Brady et al., 2003). Furthermore, 9-cis-epoxycarotenoiddioxygenase genes (involved in ABA biosynthesis) are expressedin pericycle cells surrounding LR initiation sites (Tan et al.,2003). It is tempting to suggest that ABA may restrain cellproliferation outside the LR initiation site, although ABAbeing produced as a result of the stress caused by LR emergencecannot be excluded (De Smet et al., 2006b). Indeed, ABAupregulates the expression of KRP1, a cell cycle inhibitor(Wang et al., 1998). Some auxin-induced LR-initiation geneshad previously been described as ABA-repressed (Vannesteet al., 2005). Among these, AUXIN-INDUCED IN ROOTCULTURES 12 (AIR12) and IAA19 function in LR formation(Neuteboom et al., 1999; Tatematsu et al., 2004). Thus, ABAand auxin could have an antagonistic effect on LR initiation(Fig. 4a). Interestingly, the KNAT1 homeobox transcriptionfactor is expressed at the base of LR primordia (Truernit et al.,2006) and is auxin-induced and ABA-repressed in LR pri-mordia (Soucek et al., 2007), suggesting a possible point ofintegration for the two signals. Further research is needed toestablish ABA as an inhibitor of LR initiation in Arabidopsis.

Curiously, ABA seems to stimulate LR initiation in rice (Chenet al., 2006a).

In addition to ‘classical’ plant hormones, several other signalsaffect LR development both during initiation and at laterstages, in a variety of plant species. Salicylic acid promotes LRinitiation, emergence and growth, possibly via crosstalkwith cytokinin or auxin (Echevarria-Machado et al., 2007).Melatonin promotes lateral and AR formation while decreas-ing root length, similarly to the effects of auxin (Arnao &Hernandez-Ruiz, 2007). Alkamides are lipid-based secondarymetabolites that are novel regulators of plant growth anddevelopment (Lopez-Bucio et al., 2006). They induce LRinitiation and growth in Arabidopsis (Ramirez-Chavez et al.,2004), and regulate meristematic activity throughout the plant.It is suggested that they regulate root pericycle cell activation,possibly via cytokinin signalling (Lopez-Bucio et al., 2007).

Hormone-independent signalling pathways that regulatelateral root initiation The best-characterized protein thatregulates LR initiation, independently of hormone signalling,is ABERRANT LATERAL ROOT FORMATION 4 (ALF4).The Arabidopsis alf4 mutant shows a complete absence of LRs,even in the presence of auxin (Celenza et al., 1995). Cellsappear to be blocked at a premitotic stage of the cell cycle,but the identity of the xylem pole pericycle itself is notcompromised. ALF4 is a nuclear-localized protein of unknownfunction; a shorter protein generated by alternative splicinglocalizes to the cytoplasm. Importantly, auxin has no effect onALF4 levels or intracellular localization (DiDonato et al.,2004). In the current model, ALF4 maintains the pericycle ina ‘competent’ state for cell division, allowing input from otherLR-inducing signals, including auxin (DiDonato et al., 2004).The alf4 mutant maintains full responsiveness to auxininhibition of PR elongation, suggesting that LR formation isnot a simple recapitulation of the developmental programproducing PRs.

Other regulators of LR initiation, acting independently ofknown pathways, are ARABIDILLO-1 and ARABIDILLO-2,which act redundantly to promote LR initiation in Arabidopsis(Coates et al., 2006). ARABIDILLOs are F-box proteins,suggesting that they form ubiquitin E3 ligases. Importantly,arabidillo mutants and ARABIDILLO-overexpressing plantsare able to respond to exogenous auxin similarly to wild-typeplants. In addition, auxin distribution in the root tip appearsto be normal in arabidillo mutants, and auxin does not affectthe nuclear localization of ARABIDILLO proteins (Coateset al., 2006; C. Nibau, J. Coates, unpublished).

Transcriptomic comparison of wild-type, arabidillo mutantand ARABIDILLO-overexpressing roots reveals changes insome genes defined as pericycle-enriched and LR-enriched(Birnbaum et al., 2003; Levesque et al., 2006; https://www.genevestigator.ethz.ch/), but no strong overlaps withother recent LR data sets defined by auxin induction, VFBsignalling, LR emergence or red light signalling (Vanneste

https://www.genevestigator.ethz.ch/

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et al., 2005; Laskowski et al., 2006; Molas et al., 2006;Schwager et al., 2007; J. Coates, unpublished). ARABIDIL-LOs might act very early in determining pericycle cell fate.Given the recent suggestion that this determination occurs atthe basal meristem (section III.1 ‘Which pericycle cells?’) itwill be interesting to establish whether arabidillo mutants areaffected in this process.

2. Redifferentiation to form a new meristem that recapitulates the root organization

Lateral root primordium formation and emergence A seriesof well-characterized cell divisions gives rise to the LRP(Malamy & Benfey, 1997). The coordinated pattern of celldivision is dependent on auxin signalling and on the activityof the PUCHI gene. PUCHI is expressed in pericycle cells thatwill form the LRP and in the LRP itself. PUCHI encodes anAPETALA2 (AP2) transcription factor that is upregulated byauxin and acts downstream of auxin to restrict the area of cellproliferation within the LRP. PUCHI is also necessary forcorrect cell divisions within the LRP (Hirota et al., 2007). Inrice, the EL5 RING finger ubiquitin E3 ligase maintainscell viability in the developing primordium. EL5 may actdownstream of auxin, cytokinin and JA to prevent meristematiccell death (Koiwai et al., 2007). The identity of the targetproteins and the involvement of EL5 in LRP hormonesignalling pathways remain to be investigated.

Once an LRP has initiated, it must form a functionalmeristem and emerge from within the parent root tissues. Asa result of rounds of cell division, the LRP increases in size,forming a dome-shaped structure that penetrates the externalcell layers of the PR. This requires separation of cells in theendodermis, cortex and epidermis for the passage of the LR tothe outside (Fig. 4c,d). This process must be tightly regulated,as cell separation (particularly of the protective epidermallayer) constitutes a risk to the plant, potentially allowing theentry of pathogens from the soil into internal tissues.

Much less is known about how LRs emerge than how theyinitiate. Changes in electrical potential occur around prospectivesites of LR emergence (Hamada et al., 1992) and auxin seemsto be required for LR emergence independently of its rolein LR initiation. Shoot-derived auxin is required for LR emer-gence in Arabidopsis until c. 10 d after germination (Bhaleraoet al., 2002), and auxin can induce root cell separation inArabidopsis (Boerjan et al., 1995; Laskowski et al., 1995).

Cell separation occurs via regulated activity of cell wall-remodelling enzymes. Breakdown of pectin is particularlyimportant for cell separation, as the middle lamella betweenadjacent cells is pectin-rich. Pectin is demethylated by pectinmethylesterases (PMEs) before its catabolism. Pectin breakdowninvolves homogalacturonases called pectate lyases (PLAs).Interestingly, during LR emergence, the pectin in the emergingLR remains methylated, whereas the pectin in the overlyingparent root tissues becomes demethylated, possibly in prepa-

ration for its controlled breakdown as LRs emerge (Laskowskiet al., 2006). How this differential pectin methylation is fullycontrolled remains an intriguing question.

Various Arabidopsis studies have shown that cell wall-remodelling enzymes are induced by auxin in roots (Neuteboomet al., 1999; Himanen et al., 2004; Vanneste et al., 2005;Laskowski et al., 2006). Cell wall remodelling genes inducedby auxin include a PME, PLAs, and also an expansin and abeta-xylosidase (Laskowski et al., 2006). AtPLA1 and AtPLA2are both upregulated steadily for up to 24 h after only a 15-minpulse of auxin: this response is blocked in the slr1/iaa14mutant. In addition, expression of both AtPLAs is muchhigher in LR initials than in the pericycle cells from whichthey arise (Laskowski et al., 2006).

The polygalacturonase (PG) family of cell wall-degradingenzymes may help to ‘prime’ the PR cells to separate ready forLR emergence (Gonzalez-Carranza et al., 2007). An ArabidopsisPG (PGAZAT) is expressed specifically in the cortical andepidermal cells overlying the future site of LR emergence. Apgazat insertion mutant has no obvious LR phenotype, but itis likely that functional redundancy exists. Interestingly, rootPGAZAT expression is auxin-inducible (Gonzalez-Carranzaet al., 2007).

Activation of the lateral root meristem and lateral rootelongation Activation and maintenance of the LR meristemrequires polarized auxin transport to create an auxin maximumat the tip of the LRP: this requires regulated activity of auxininflux and efflux transporters. During LR development thereis an important change in the direction of auxin flow, broughtabout by AUX/IAA-dependent repositioning of auxin effluxcarriers towards the tip of the newly formed LR. This resultsin LR growth perpendicular to the PR (Benkova et al., 2003;Sauer et al., 2006). The new LRP auxin maximum regulatesthe activity of several transcription factors (Blilou et al., 2005).It is proposed that regulated expression of known regulatorsof PR meristem formation, such as the PLETHORA,CLAVATA, SCARECROW and SHORT ROOT, is alsoimportant for the maintenance of an active meristem in LRsdownstream of auxin (for a recent review see Scheres, 2007).Because mutations in these genes severely impair PR growth,their effect on LR development has not been investigated:targeted overexpression and underexpression in LRs willclarify this issue.

Abscisic acid can reversibly block meristem activationpostemergence by inhibiting the cell cycle gene expressionnecessary for meristem activity, leading to LR growth arrest(De Smet et al., 2003). This effect of ABA defines a newauxin-independent checkpoint between LR emergence andmeristem activation, which may also be regulated by nitratelevels (De Smet et al., 2003). In line with this observation, anABA receptor mutant is completely insensitive to ABA inhi-bition of LR development (Razem et al., 2006). No otherknown ABA-insensitive mutants show insensitivity, suggesting

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that ABA signalling during LR emergence involves specificproteins (De Smet et al., 2003). ABI8, a plant-specific proteinof unknown function, is a possible novel signalling candidate.abi8 mutant plants are less sensitive to ABA and, despitebeing able to initiate LR, their LR meristem soon losescompetence to divide (Cheng et al., 2000; Brocard-Giffordet al., 2004).

This checkpoint between LR emergence and meristemactivation provides an elegant way by which environmental,nutritional and endogenous factors can modulate root archi-tecture through ABA signalling (Signora et al., 2001; De Smetet al., 2006b; and section IV). For example, stress-inducedoxylipin production affects LR development. Treatment ofArabidopsis seedlings with 9-hydroxyoctadecatrienoic acid(9-HOT), an oxylipin derivative, induces the accumulation ofarrested early stage LRPs, accompanied by the upregulationof cell wall-associated genes (Vellosillo et al., 2007). Thenot-responding to oxylipins2 (noxy2) mutant has more LRsthan the wild-type plant. 9-Hydroxyoctadecatrienoic acid andrelated oxylipins are probably endogenous modulators ofLR emergence that may act via ABA signalling and they areinvolved in RSA reprogramming in response to pathogeninfection (Vellosillo et al., 2007).

Interestingly, ABA appears to have the opposite effect onLR emergence in legumes, stimulating LR formation inMedicago (Liang & Harris, 2005). The Medicago latd mutanthas a reduced root surface area with short PRs, arrested LRPsand disorganized meristems (Bright et al., 2005). The latdphenotype can be at least partly rescued by the exogenousapplication of ABA, and latd mutants seem to be impaired inABA perception or signalling (Liang et al., 2007).

Lateral root elongation occurs by cell division and elongationfrom the meristem and is controlled by several factors. Auxintransport and signalling are important in this process. Auxintransport within the root is necessary for LR elongation, as

mutations in the auxin efflux transporter MDR1 cause nascentLRs to arrest their growth (Wu et al., 2007). The ALF3 proteinelevates the levels of auxin at the LRP, probably by facilitatingauxin transport (Celenza et al., 1995). The auxin-inducedhomeobox gene HAT2 may also modulate auxin distributionwithin the primordium (Sawa et al., 2002).

Despite the fact that cytokinins inhibit LR initiation, theyhave a positive effect on LR elongation in Arabidopsis and rice,possibly via stimulation of cell cycle gene expression in anauxin-independent process (Rani Debi et al., 2005; Li et al.,2006b).

IV. Plasticity: modification of lateral root development by the environment

Plants are sessile organisms that need to survive in a dynamicenvironment. Consequently, their root systems need tomaintain plasticity to react to fluctuating abiotic and bioticfactors. Genetically identical plants can have very differentRSA when grown in varying environmental conditions. Plantsprimarily respond to the abundance of macronutrients andwater to produce the best root network for optimum growthand survival (Fig. 5). However, other exogenous factors, suchas plant–pathogen interactions, are also important for rootdevelopment. An overview of the current understandingof how changing external conditions affect RSA is presentedhere, with a particular focus on more recent advances.

1. Nitrogen availability and root system architecture: local and global effects

Inorganic nitrogen Root adaptation to nitrogen levels is anexcellent example of a plants’ developmental plasticity. Nitrogenis available in the soil as ammonia, nitrite, nitrate and organicnitrogen. The abundance of these compounds is highlyvariable and can have dramatic effects on LR development.Species-specific differences in nitrogen responses are apparent:LR length, number or both can be affected (Zhang & Forde,1998; Linkohr et al., 2002; Boukcim et al., 2006).

Nitrate levels have strongly opposing effects on LR growth,depending upon the context in which they occur. In low-nitratesoils, patches of high nitrate have a localized stimulatory effecton LR development in many species (Drew & Saker, 1975;Zhang & Forde, 1998). However, where nitrate levels areglobally high (i.e. not growth limiting), LR growth is inhibited(Zhang et al., 1999). Thus, there are two clear morphologicaladaptations: a local stimulatory effect of exogenous nitratesupply on LR elongation, and a systemic inhibitory effect ofhigh nitrate on LR meristem activation. This is caused by thesignalling effect of nitrate itself, rather than being a responseto downstream metabolites (Zhang & Forde, 1998). Somespecies, including barley and cedar, but not Arabidopsis, arealso able to respond to a localized ammonium supply (Drew,1975; Zhang et al., 1999; Boukcim et al., 2006).

Fig. 5 Lateral root responses to nutrient deprivation. When nitrate (N) levels are high, lateral root (LR) emergence and elongation is represssed compared with normal conditions. Locally high levels of N promote local LR proliferation. In low phosphate (P), primary root growth ceases and LR density increases. In low sulphate (S), primary root growth and lateral root density increase, with LRs originating closer to the root tip. In low potassium (K), LR elongation is inhibited.

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Key protein players specific to the ‘local nitrate’ responseinclude the Arabidopsis NITRATE REGULATED-1 (ANR1)MADS-box transcription factor and the DUAL AFFINITYNITRATE TRANSPORTER (AtNRT1.1). Downregulationof ANR1 reduces LR stimulation in nitrogen-rich zones,without compromising the overall nitrate-induced inhibitionof LRs (Zhang & Forde, 1998). Seven other MADS box geneshave a similar expression pattern to ANR1 under differentnitrate conditions (Gan et al., 2005). Three of these (AGL-16,AGL-21 and SOC1) interact with ANR1, although whetherthey represent nitrate signal transduction components isunknown (de Folter et al., 2005).

AtNRT1.1 is induced by nitrate (Munos et al., 2004) andAtnrt1.1 mutants exhibit a strongly decreased response tolocal nitrate supply (Liu et al., 1999). Interestingly, thisreduced responsiveness is accompanied by a reduction ofANR1 mRNA (Remans et al., 2006). Transporters have beenpreviously identified as nutrient sensors, but it is unclearwhether AtNRT1.1 is involved directly in nitrate sensing, orin facilitating access of nitrate to another sensor.

High nitrogen inhibits LR development after emergencebut before meristem activation. This effect is reversible: trans-ferring plants to nitrate-limiting media results in a release ofLR inhibition within 24 h, so plants can respond rapidly tofluctuating environmental nitrate levels (Zhang & Forde,1998). A high shoot nitrate status is important for the inhib-itory response, and an Arabidopsis mutant lacking nitratereductase activity is hypersensitive to inhibition, suggestingthat systemic accumulation of nitrate causes LR inhibition(Zhang et al., 1999).

How are nitrate responses regulated during LR development?Various ABA-deficient Arabidopsis mutants have significantlyreduced levels of LR inhibition in abundant nitrate (Signoraet al., 2001). With both ABA and high nitrate, LRs are inhibitedimmediately after meristem activation (Signora et al., 2001;De Smet et al., 2003; and section III.1 ‘Other hormonesaffecting LR development’). Arabidopsis LR ABA-insensitive(LABI) mutants can still produce LRs in the presence of ABA:they are also less sensitive to high nitrate, implying that theinhibition of LRs by ABA and nitrate involves the samemechanism (Zhang et al., 2007a). Interestingly, transferringArabidopsis and soybean from conditions of high nitrate tolow nitrate increases root auxin (IAA) levels, suggesting thatnitrate affects auxin synthesis or transport (Caba et al., 2000;Walch-Liu et al., 2000).

Carbon : nitrogen (C : N) ratios affect RSA, further high-lighting the complexity of the root response to nitrate. A highsucrose : nitrate ratio suppresses LRs, and a mutation in thehigh-affinity nitrate transporter AtNRT2.1 abolishes thisinhibition (Malamy & Ryan, 2001; Little et al., 2005). LikeAtNRT1.1, AtNRT2.1 may be a direct nitrate sensor (Littleet al., 2005). In addition, AtNRT2.1 may have differentfunctions depending on the degree and context of nitratedeficiency (Remans et al., 2006).

Organic nitrogen Plants can use both organic nitrogen andinorganic nitrogen as a nutrient source. Arabidopsis roots showa specific set of responses to the amino acid l-glutamate,which inhibits PR growth and causes concomitant increases inLR density to varying degrees in different ecotypes (Walch-Liuet al., 2006). This response is similar to roots grown in lowphosphate, forming a short and highly branched RSA (sectionIV.2; Williamson et al., 2001; Walch-Liu et al., 2006).Root responses to l-glutamate are accompanied by dramaticcytological changes, including microtubule depolymerization(Sivaguru et al., 2003).

The PR tip is the sensor for l-glutamate (as with phosphate;section IV.2), which inhibits cell division in the meristem(Walch-Liu et al., 2006). Interestingly, the auxin transportmutant aux1 is somewhat insensitive to l-glutamate, whereasthe axr1 mutant (a modifier of auxin signalling and possiblyalso other hormone pathways) is hypersensitive to l-glutamate,and various other auxin-signalling mutants exhibit wild-type sensitivity to l-glutamate (Walch-Liu et al., 2006). l-glutamate probably acts as a signalling molecule rather thanas a nutritional cue, because closely related amino acids do notelicit changes in root architecture (Walch-Liu et al., 2006).The molecular mechanism of l-glutamate perception at theArabidopsis root tip remains to be discovered. Interestingly,rice with a mutant putative glutamate receptor (OsGLR3.1)has short PRs and LRs, reduced cell division, and prematuredifferentiation and cell death in the root meristem (Li et al.,2006a).

Carnitine, an organic nitrogenous cation, induces LRformation. However, disruption of an Arabidopsis plasmamembrane-localized carnitine transporter, AtOCT1, ledto increased root branching (Lelandais-Briere et al., 2007).AtOCT1 promoter activity is present in the root vasculature,including at sites of LR initiation. This suggests a possiblemodulatory role for carnitine movement or homeostasis in thecontrol of RSA. It seems that AtOCT1 negatively regulates LRdevelopment, and the local concentration of carnitine in theroot may affect the C : N ratio and hence LR development(Lelandais-Briere et al., 2007).

2. Phosphorous: modulating total RSA but sensed at the root tip

Phosphorous is an essential nutrient, primarily taken up viathe roots as inorganic phosphate (Pi). Phosphate is one of themost inaccessible macronutrients in the soil, as it formsinsoluble compounds with metals in acidic and alkaline soils(Raghothama, 1999). Root system architecture modificationsin response to phosphate are critical for the fitness of the plantand differ from those seen with nitrate, perhaps reflecting aPi-foraging strategy, in contrast to nitrate responses thatimprove nitrogen uptake (Fitter et al., 2002).

The main adaptive trait for accessing phosphate is the abilityto explore different layers near the soil surface through

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changes in the RSA (Lopez-Bucio et al., 2000). Variousadaptations have evolved in different plants. In Arabidopsis, Pideficiency favours a redistribution of growth from the PR toLRs. The PR stops growing and the density and elongation ofLRs increases, forming a shallow, highly branched root system(Williamson et al., 2001; Lopez-Bucio et al., 2002). Thisprevents further growth into less nutrient-rich deeper soils,increasing the exploration of the more nutrient-rich upperstrata. In the bean Phaseolus vulgaris, a different strategy hasevolved for achieving a similar explorative result: the angle ofroot growth is shifted to predominantly outwards instead ofdownwards when Pi levels are low (Bonser et al., 1996). Thenitrogen-fixing white lupin forms proteoid (cluster) roots thatsecrete organic acids and phosphatases into the surroundingsoil to solubilize phosphate and aid its uptake (Schulze et al.,2006).

Unlike nitrate responses, the initial effect of low-Pi sensingis the arrest of PR growth, with changes in LRs occurring later.Loss of PR growth occurs via reduced cell elongation and aprogressive loss of meristematic activity (Williamson et al.,2001; Sanchez-Calderon et al., 2005). The phosphate deficiencyresponse-2 (pdr2) mutant displays hypersensitive inhibition ofcell division in developing root meristems under Pi-limitingconditions, suggesting that PDR2 is required for meristemfunction where external Pi is low. It therefore represents aPi-sensitive checkpoint that monitors Pi status and allows theroot system to adjust accordingly (Ticconi et al., 2004). Inaddition to soil Pi status, systemic Pi levels may also beimportant for the induction of Pi-deficient RSA responses(Williamson et al., 2001). Active photosynthesis, or thepresence of sugar, is also essential for RSA responses to limitingphosphate (Karthikeyan et al., 2007).

Physical contact of the Arabidopsis PR tip with low-Pimedium is necessary and sufficient to arrest primary growthand reprogram root architecture (Svistoonoff et al., 2007).Multicopper oxidase mutants LOW PHOSPHATE ROOT-1and -2 (LPR-1/-2) form long PRs in low Pi and provideevidence that the root cap has an important role in nutrientsensing. Interestingly, LPR1 was previously identified as aquantitative trait locus (QTL) important for phosphateresponses (Reymond et al., 2006). Despite highlighting anovel role for multicopper oxidases in plant development, it isunknown whether LPRs are directly involved in the stimulationof LR growth in low Pi.

A variety of hormones may modify the Pi response.Responses to low Pi correlate with increased auxin sensitivityand changes in auxin transport (Lopez-Bucio et al., 2002; Jainet al., 2007). Low phosphate resistant (lpr) mutants of BIG, aprotein required for wild type levels of auxin transport, havereduced LRs in low Pi (Gil et al., 2001; Lopez-Bucio et al.,2005). However, neither BIG nor auxin transport is requiredfor other RSA modifications seen in low Pi (Lopez-Bucioet al., 2005). Interestingly, many root responses to phosphatestarvation are repressed by cytokinin signalling (Franco-Zorrilla

et al., 2005). In addition, Pi starvation affects gibberellinsignalling in roots, whereas gibberellin can attenuate thelow-Pi response (Jiang et al., 2007).

A variety of protein regulators of the phosphate-deficiencyresponse have been uncovered, which affect transcription,translation and post-translational modifications. PHOS-PHATE STARVATION RESPONSE-1 (PHR1) is an Arabi-dopsis MYB-like transcription factor that regulates a numberof Pi-deficient responsive genes and is conserved in variousplant species (Rubio et al., 2001). Miura et al. (2005) reportedthat PHR1 is a target of the small ubiquitin modifier (SUMO)E3-ligase AtSIZ1 in vitro. Interestingly, Atsiz1 mutants exhibitan exaggerated response to low Pi levels compared with wildtype, most notably an extensive increase in LR developmentand a stronger PR inhibition (Miura et al., 2005). Althoughno direct link between PHR1 and RSA modification has beenshown, two genes that belong to the PHR1 regulon (AtIPS1and AtRNS1) are positively regulated by AtSIZ1 during theinitial stages of Pi limitation (Miura et al., 2005). However, itis unknown whether the root phenotype of Atsiz1 mutants isa result of PHR1 modification and subsequent downstreamgene expression, or whether the effect is pleiotropic, as AtSIZ1also has roles in other developmental pathways (Jin et al.,2008).

Other transcription factors identified, but not fully charac-terized as Pi-response components, include the basic leucinezipper (bZIP) transcription factor, PHI-2, in tobacco, andmore recently OsPTF1, a bHLH transcription factor providingtolerance to low-Pi conditions in rice (Sano & Nagata, 2002;Yi et al., 2005). The WRKY75 transcription factor is stronglyinduced during Pi deprivation (Devaiah et al., 2007). Severalgenes are downregulated in plants with reduced levels ofWRKY75, including high-affinity Pi transporters, whichconsequently leads to reduced phosphate uptake during Pistarvation (Devaiah et al., 2007). WRKY75 may be a specificmodulator of LR development (rather than affecting the PR)and may also act independently of the Pi status of the plant tomodify LR development (Devaiah et al., 2007).

3. Root responses to sulphur

Sulphur, in the form of sulphate, is required for the synthesisof methionine and cysteine and is critical for cellularmetabolism, growth and development, and stress responses.Sulphate deficiency is detrimental to a plant’s survival andleads to the development of a prolific root system, usually atthe expense of shoot growth (Kutz et al., 2002). Sulphate-deficient roots elongate faster than those with sufficientsulphate, with LRs developing earlier, closer to the root tipand at a greater density (Kutz et al., 2002). This leads to anincrease in total root surface area and a greater exploration ofthe soil.

Sulphur deprivation leads to transcriptional activation ofNITRILASE3 (NIT3), which converts indole-3-acetonitrile

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(IAN) to auxin (Kutz et al., 2002). Low sulphate-inducedLRPs exhibit high NIT3 promoter activity, thus generatingadditional auxin close to the pericycle, allowing increased LRinitiation (Kutz et al., 2002). Sulphur deficiency also upregulatesthe sulphate transporter genes SULTR1;1 and SULTR1;2 inthe epidermis and cortex of roots (Yoshimoto et al., 2002); bothtransporters are reversibly downregulated in sulphate-repleteconditions (Maruyama-Nakashita et al., 2004). A sulphurresponse regulatory element (SURE) is conserved in theupstream region of a variety of sulphate-deficient responsegenes, suggesting that RSA alterations in response to sulphurlevels are coordinately controlled in Arabidopsis roots(Maruyama-Nakashita et al., 2004).

Interestingly, SURE regions contain ARF consensussequences, suggesting a role for auxin in the early sulphate-starvation response (Maruyama-Nakashita et al., 2004). Anumber of AUX/IAA genes have been implicated in the sul-phate response, and transcriptomic analysis suggests that bothauxin influx and IAA28 activity may modulate the response tolow sulphate, perhaps by acting in a negative regulatory manner(Nikiforova et al., 2003, 2005). More recently, (Dan et al.,2007) suggested that auxin is involved in a subset of sulphur-deficiency responses, with other hormones (such as cytokininand ABA) also playing a role. SULTR1 mRNA accumulationcan be reduced by exogenous cytokinin, further suggestingpoints of regulation (Maruyama-Nakashita et al., 2004).

4. Potassium and lateral root development

Lateral roots of potassium-starved plants arrest their elongation(Armengaud et al., 2004). Analysis of root transcriptomesfrom potassium-starved seedlings which were then resuppliedwith potassium revealed that certain genes were downregulatedby potassium resupply, including stress-induced genes,transporters, calcium signalling components, sulphurmetabolism components, and cell wall-remodelling enzymes.Conversely, upregulated genes were either transporters(including three root-specific nitrate transporters) or cell wall-remodelling enzymes. The transcriptomic profile of potassium-starved plants overlaps with sulphur starvation, but not withnitrate starvation or phosphate starvation, and also involveschanges in jasmonate/defence signalling (Armengaud et al.,2004). Interestingly, the MYB77 transcription factor providesa direct link between potassium starvation responses andauxin signalling (Shin et al., 2007).

5. Water and salt stresses

Water stress Water availability has a profound effect on aplant’s root system. Plant roots will grow towards wetter soiland away from high osmolarity (Takahashi et al., 2003). Aswater availability decreases (or osmotic stress increases), LRemergence is repressed, although LR initiation is largelyunaffected (van der Weele et al., 2000; Deak & Malamy,

2005; Xiong et al., 2006). This is likely to be an adaptiveresponse encouraging increased water uptake from deeper soillayers. The molecular mechanisms underpinning the responseare largely unknown, although ABA has an important role.The ABA-deficient mutants aba2-1 and aba3-2 have increasedroot system size compared with wild type under high osmotica(Deak & Malamy, 2005). Plants mutant for the LATERALROOT DEVELOPMENT 2 (LRD2) and ArabidopsisCYTPOLASMIC INVERTASE (AtCYT-INV1) genes alsohave a similar phenotype (Deak & Malamy, 2005; Qi et al.,2007). Alongside ABA, LRD2 may be required to determinethe percentage of LRPs that become LRs under normal andstress conditions (Deak & Malamy, 2005).

Abscisic acid and drought stress have similar and probablysynergistic effects on LR development. Several drought inhibitionof lateral root growth (dig) mutants have enhanced responses toABA and are also drought tolerant, whilst others have areduced LR-inhibition response to ABA and are droughtsensitive (Xiong et al., 2006). DIG3 is particularly importantfor LR inhibition in response to ABA: dig3 mutants havenormal LR growth under stress and are susceptible to drought.Interestingly, dig3 plants were smaller than wild-type plantsunder well-watered conditions, suggesting that the ABA anddrought response involves factors required more generally forgrowth (Xiong et al., 2006). Drought tolerance in crop speciesis controlled by multiple QTLs (Nguyen et al., 2004): it willbe interesting to discover whether dig loci define drought-tolerant QTLs that are important for responding to water-stressin roots and globally.

Salt stress Salt stress, which is related to drought stress, alsoreprograms RSA. Salt stress in Arabidopsis can induce rootswelling with shorter total root lengths, a seriously reducedmeristematic zone and a strong reduction in the number ofLRPs, accompanied by the downregulation of several cell cyclegenes (Burssens et al., 2000). However, salt stress may alsotrigger an increase in LR number. In chickpea (Cicer arietinum),the CAP2 (C. arietinum AP2) transcription factor is inducedupon dehydration and binds to dehydration-response elementsin many stress-inducible genes (Boominathan et al., 2004;Shukla et al., 2006). Transgenic tobacco expressing CAP2 istolerant to salinity and osmotic stress, possibly because of alarge increase in LR number (Shukla et al., 2006). Manyauxin-response genes associated with LR development areupregulated in these plants, indicating links between salt stressresponses and intrinsic auxin-associated development (Shuklaet al., 2006).

He et al. (2005) reported increased LR numbers and areduction of PR length in response to high levels of NaCl inArabidopsis. The NAC2 transcription factor is upregulated byNaCl and its overexpression causes increased LR formationspecifically without a change in root length (He et al., 2005).NAC2 is upregulated by ethylene, auxin and ABA, and itsinduction by salt is compromised in auxin and ethylene

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signalling mutants (He et al., 2005). These data highlight theimportance of phytohormone signalling in RSA responses tosalinity.

6. Effects of light on root architecture

Responding to light is key to plant survival. In addition tohaving profound effects on the seed and shoot, light can affectLR morphology. This can be direct (e.g. red light enhances LRformation via the COL3 gene) (Datta et al., 2006) or indirect,via effects in the shoot (Bhalerao et al., 2002).

The bZIP transcription factor LONG HYPOCOTYL 5(HY5) is a key player in light-induced development in Arabi-dopsis (Koornneef et al., 1980). Initially noted for defectivelight-induced hypocotyl elongation, hy5 mutants also have anelevated number of LRs, which grow faster than wild-typeroots and are less responsive to gravity (Oyama et al., 1997).The hy5 root phenotype occurs as a result of the underexpres-sion of two negative regulators of the auxin signalling pathway:AUXIN RESISTANT 2 (AXR2)/IAA7 and SOLITARYROOT (SLR)/IAA14 (see section III.1 ‘Lateral root initiationrequires auxin and regulated protein degradation’; Cluis et al.,2004). This interaction between HY5 and auxin signallinghighlights the importance of both light-signalling networksand hormone-signalling networks in the control of RSA. HY5also interacts with SALT TOLERANCE HOMOLOGUE 2(STH2) (Datta et al., 2007). The sth2 mutant phenocopiesthe exaggerated root phenotype of the hy5 mutant, andthe authors suggest that light-dependent inhibition of LRsby STH2 requires its binding to HY5, where it providestransactivating potential to the transcription factor (Dattaet al., 2007).

HY5 HOMOLOGUE (HYH) is a functional equivalent ofHY5 with a similar expression pattern and responsiveness tolight (Sibout et al., 2006). hyh mutants show wild-type RSA.However, hy5 hyh double mutants exhibit a suppression ofthe hy5 phenotype, displaying less prolific root growth thanwild type (Sibout et al., 2006). It has been proposed thatthese double mutants represent the morphological responseto a quantitative gradient in auxin signalling. This examplesuggests that the inactivation of genes, both of which affectthe balance of a physiological process in the same manner, canresult in very different morphological changes (Sibout et al.,2006).

Molas et al (2006) examined total gene expression indark-grown roots that were treated with red light for just 1 h.Interestingly, genes affecting cell wall metabolism and remod-elling were consistently downregulated. Genes involved inhormone signalling (auxin, GA, ethylene) were also affected,as were proteins involved in intercellular transport, varioustranscription factors and several F-box proteins (Molas et al.,2006). Thus, light-induced changes in RSA are likely tohappen rapidly and involve both signalling and remodellingprocesses.

7. Modulation of root architecture by biotic factors

Within the soil, plants must compete and interact with aplethora of organisms, including microorganisms and otherplant root systems. Roots secrete chemicals into the soil thataffect other plant RSAs and also influence communicationwith microorganisms (Bais et al., 2004). In turn, viruses,bacteria and fungi can modify RSA. Many of these interactingspecies are pathogens and result in plant defence responses,while some can form symbiotic interactions leading to theformation of root nodules or mycorrhizas/proteoid roots(Autran et al., 2006; Oldroyd & Downie, 2006). In addition,soil microorganisms can produce auxin and cytokinin thatdramatically affect RSA (see Section III) (Costacurta &Vanderleyden, 1995). Some recent advances in the molecularunderstanding of how pathogens modify RSA are presentedin the following sections.

Viral proteins Cucumber mosaic virus (CMV) infects a rangeof dicots, inducing developmental and growth abnormalities.The severity of disease symptoms is dependent on theCMV-2b protein (Lewsey et al., 2007). CMV-2b bypasseshost defences both by inhibiting plant RNA silencingmechanisms (thus promoting the undetected spread of viralRNA) and by antagonizing salicylic acid signalling, whichnormally inhibits viral replication and cell-to-cell spreading.Arabidopsis infected with CMV or overexpressing CMV-2bshow perturbed RSA, specifically, shorter PRs, increased LRdensity and increased LR length, leading to increased rootsurface area (Lewsey et al., 2007). Interestingly, CMV-2bstabilizes a number of endogenous Arabidopsis mRNAs thatare targets of degradation by microRNAs (miRNAs), includingthe auxin signalling genes ARF17 and NAC1. Curiously,stabilized ARF17 is proposed to inhibit LR formation (Malloryet al., 2005), whereas NAC1 promotes LR development (Xieet al., 2000), suggesting that targeting of NAC1 may beparticularly relevant during CMV infection. Cucumbermosaic virus ultimately inhibits root growth, but it is possiblethat transient increases in LR formation upon CMV infectionare advantageous during initial virus infection and spread,because the presence of a higher number of emerging LRs andan increase in root surface area could provide a greater numberof sites for virus entry.

Pathogenic bacteria and fungi Pathogenic bacteria and fungican directly influence LR development. Ralstonia solanacearuminoculation leads to reduced formation and elongation of LRsin petunia (Zolobowska & Van Gijsegem, 2006). Novel rootlateral structures develop, derived from the pericycle foundercells that normally form LRs. These seem to act as colonizationsites, and this process probably requires secreted bacterialproteins (Zolobowska & Van Gijsegem, 2006).

The bacterium Pseudomonas syringae stimulates LRdevelopment and other auxin-related changes in Arabidopsis,

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whereas exogenous auxin promotes disease progression (Chenet al., 2007). The authors suggest that auxin could promotecell wall loosening. A Pseudomonas peptide was reported todownregulate auxin signalling, enabling disease resistance;however, the effect on LR development was not investigated(Navarro et al., 2006). The rice transcription factor OsWRKY31is induced by rice blast fungus and also by auxin. Overexpressionof OsWRKY31 confers resistance to rice blast fungus infectionand also inhibits LR formation (Zhang et al., 2007b) In addition,OsWRKY31 upregulates auxin responsive genes, again linkingauxin signalling and/or transport with the defence response(Zhang et al., 2007b).

Interestingly, the nitrate-inhibitory effect on LR developmentis over-ridden when plants are inoculated with Phyllobacterium,a growth-promoting rhizobacterium (Mantelin et al., 2006).This effect was accompanied by altered expression of varioustransport genes, including AtNRT1.1.

Continuing research in this new area will define the extentto which plant–pathogen interactions affect RSA.

V. Transcriptomic studies to identify potential new regulators of lateral root development

With the advent of high-throughput ‘omic’ experimentaltechniques, it is possible to augment molecular geneticstudies of LR developmental mechanisms. This has includedthe generation of data sets of genes that are upregulatedor downregulated specifically in different root cell typesor in response to specific signals (see various sectionsabove).

In terms of probing cell type-specific gene expression inroots, studies from the Benfey laboratory have been influential.An initial study identified several hundred genes enriched invascular tissues, including pericycle (Birnbaum et al., 2003).More recently, a high-resolution gene-expression map ofall root cell types, including pericycle, xylem pole pericycle,phloem pole pericycle and LRPs, has been created (Bradyet al., 2007). Analysis of this vast data set will provide newinsights into the gene regulation occurring during LRdevelopment. For example, pericycle (in particular xylem polepericycle) is enriched in mRNAs encoding cell wall-modifyingenzymes, whereas genes encoding kinases and enzymes requiredfor cell wall loosening are enriched in LRPs. In addition, auxinbiosynthetic genes are enriched in pericycle and LRPs, andABA signalling components are enriched in pericycle (Bradyet al., 2007).

A meta-analysis identifying indirect targets of the SHOR-TROOT (SHR) transcription factor uncovered a number ofSHR-regulated genes that were enriched in or exclusive topericycle (Levesque et al., 2006). It is thus tempting to specu-late that SHR signalling pathways may regulate LR formationas well as PR development (Scheres et al., 2002), especially assimilar signalling may regulate AR formation in pine trees andsweet chestnut trees (Sanchez et al., 2007).

Specific cell types have been isolated from maize roots bylaser capture microdissection (LCM) for transcriptomicand proteomic analysis (Woll et al., 2005; Dembinsky et al.,2007). Comparison of the pericycle transcriptome ofwild-type maize with that of a mutant that cannot initiateLRs revealed that the majority of differentially expressedgenes are involved in transcription or metabolism, or haveunknown function. However, several genes involved in signaltransduction (especially protein kinases), cell cycle regulation,cellular transport and defence were also identified (Woll et al.,2005).

To identify genes involved in pericycle cell fate specification,rather than LR formation per se, pericycle cells were dissectedfrom along the length of the root before the time that celldivisions occur (Dembinsky et al., 2007). The pericycletranscriptome and proteome was analysed, and furtherpericycle-enriched genes were isolated from cDNA librariesand expressed sequence tags (ESTs) (Dembinsky et al., 2007).Around 40 ‘pericycle-specific’ genes were identified, of whichthe largest two subsets were transcriptional regulators andunknown genes. Compared with vascular cells, pericycleappears enriched in genes involved in protein synthesis, butlow in genes regulating cell fate. Twenty abundant solublepericycle proteins were identified, of which 80% have a meta-bolic or energy function. There is only a small overlap betweenthe LR initiation data set (Woll et al., 2005) and the pericycledata sets (Dembinsky et al., 2007), suggesting that specifyingpericycle cell identity is a distinct process from forming anew LR.

VI. Conclusions and future challenges

A vast number of signals, both from within and outside theplant, impinge on the root to regulate its final architecture andbranching pattern. Many challenges still exist for future ‘rootbiologists’. We must understand at the molecular level howthese different signals work together to direct pericycle cellbehaviour and later LR developmental processes. We mustdiscover potentially novel signals that regulate LR develop-mental proteins which currently reside outside knownsignalling networks. There are questions we can ask about theevolution of RSA regulation across the plant kingdom. Thereare huge transcriptomic data sets that will provide us with newclues about the changes in gene expression necessary for LRdevelopment to occur. Moving our knowledge gained inArabidopsis and genetically tractable crop plants into otheragronomically relevant species will provide an understandingof how to engineer crop plants that can exist in a range ofpotentially problematic environments.

Acknowledgements

The authors thank Laurent Laplaze and Jeremy Roberts foruseful comments.

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Branching out in new directions: the control of root architecture by