Post-embryonic root organogenesisin cereals: branching out frommodel plantsBeata Orman-Ligeza1, Boris Parizot2,3, Pascal P. Gantet4,5, Tom Beeckman2,3,Malcolm J. Bennett6, and Xavier Draye1

1 Universite catholique de Louvain, Earth and Life Institute, Louvain-la-Neuve, Belgium2 Department of Plant Systems Biology, VIB, B-9052, Ghent, Belgium3 Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052, Ghent, Belgium4 Universite Montpellier 2, UMR DIADE, Montpellier, France5 IRD, LMI RICE, University of Science and Technology of Hanoi, Agronomical Genetics Institute, Hanoi, Viet Nam6 Centre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Sutton Bonington, LE12 5RD, UK

Review

The root architecture of higher plants is amazinglydiverse. In this review, we compare the lateral rootdevelopmental programme in cereals and Arabidopsisthaliana. In cereals, cells in the endodermis are recruitedto form the new root cap and overlying cortical cellsdivide to facilitate the emergence of the lateral rootprimordium. The TIR1/ABF2 auxin receptors and theAUX/IAA, ARF, and LBD transcriptional regulatory pro-teins are conserved in cereals and Arabidopsis. Severalelements of this regulatory network are common tolateral and crown roots in cereals. Also, the groundmeristem from which crown roots differentiate showssimilarities with the root pericycle. Studies in cerealspromise to give complementary insights into the mech-anisms regulating the development of post-embryonicroots in plants.

Moving from Arabidopsis to crop root systemsUnderstanding the regulation of root architecture is ofgreat agronomic importance because it is a key determi-nant for plant anchorage, efficiency of water and nutrientuptake, and establishment of plant–microorganisms com-munities. Higher plants exhibit an amazing diversity ofroot architectures at both the systems and anatomicallevel. Many dicot species such as Arabidopsis (Arabidopsisthaliana) have a primary root that iteratively branches togenerate several orders of lateral roots, whereas the rootsystem of cereal crops such as barley (Hordeum vulgare),maize (Zea mays), and rice (Oryza sativa) is predominantlycomposed of many shoot-borne crown roots that branchsequentially to form a herringbone-like structure (Box 1)[1]. Despite this apparent morphological diversity, recentgenetic studies have identified many genes that are com-mon to the formation of shoot-borne crown roots and root-borne lateral roots in cereals [2,3].

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Corresponding author: Draye, X. (xavier.draye@uclouvain.be)Keywords: root system architecture; hormones; rice; maize; barley; cereals.

Crown and lateral root formation in cereals encom-passes the suite of post-embryonic developmental process-es by which new roots arise from a shoot node or fromprimary, seminal, adventitious, and other lateral roots(Box 1). The formation of crown and lateral roots leadsto an increased number of functional root meristems,which has a profound impact on root system architecture.The elongation of crown roots primarily expands the vol-ume of soil explored, whereas the formation of most lateralroots increases the absorption surface of the root system[4]. It is now widely accepted that many aspects of crownand lateral root formation, including the temporal se-quence of crown root formation, the spacing of lateral roots,and the growth rate and angle of crown and lateral roots,influence the ability of the root system to exploit differentspatial and temporal soil niches [5] and are key to optimis-ing the capture of soil resources [6,7].

Although Arabidopsis is the best-characterised experi-mental system with regards to studying lateral roots de-velopment (reviewed in [8]), impressive progress has alsorecently been made in cereal crops regarding lateral andcrown root formation. In this review, we make a compara-tive analysis of the morphology at key developmentalsteps, regulatory signals, and gene networks that drivethe lateral root developmental programme in cereals andArabidopsis (see Lavenus et al. in this issue of Trends inPlant Science for a companion review focussing on Arabi-dopsis). Although lateral roots are the main focus of thisreview, references to crown roots have been included aswell to highlight conserved elements of the crown andlateral root developmental programmes. Readers interest-ed in the environmental regulation of cereal root architec-ture are referred to the recent review by Tich and Watt [9].

Lateral root formation: variations on a themeLateral root primordia originate from a subset of cells(called founder cells) at the periphery of the stele of theparent root. In maize, rice, barley, and wheat (Triticumaestivum), founder cells originate from pericycle and endo-dermis cells located opposite phloem poles [3,10,11]. This

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Box 1. Organisation of a cereal root system

The root system of cereals is composed of different types of roots

[1,2,81] that are exemplified here by the schematic representation of a

maize seedling (Figure I). The primary root (termed ‘radicle’ in rice)

emerges from the seed quickly after germination. In the next few

days, seminal roots emerge from the scutellar node in maize, whereas

five embryonic crown roots emerge from the coleoptilar node in rice.

These roots constitute the embryonic root system, which is essential

during plant establishment and sometimes remains functional over

the whole life cycle. The largest part of the root system is made up of

shoot-borne post-embryonic roots that are produced sequentially

from the successive shoot nodes, starting at the coleoptilar node.

These adventitious roots, which are part of the normal development

plan of cereals, are designated crown roots or nodal roots.

Adventitious emerging above the soil surface are designated brace

roots (e.g., in maize). In rice, hundreds of crown roots are formed

within 6 weeks after germination. Depending on the genotype, crown

roots have a relatively large diameter and elongation rate, an

indeterminate growth type, and positive gravitropism.

Over their entire life, primary, seminal, and crown roots initiate

lateral roots in a regular acropetal sequence, although branching

patterns are often obscured in field conditions by growth responses

to local soil conditions [121]. Lateral roots in cereals vary in terms of

diameter, growth rate and duration, branching angle, and tropism. In

rice, the lateral root population comprises long and thick lateral roots

(lLRs) with gravitropic and indeterminate growth and short and tiny

lateral roots (sLRs) with agravitropic and determinate growth [2],

whereas maize and barley produce a continuum of lateral root types

[22]. Strong lateral roots (or lLRs in rice) also have the ability to

produce lateral roots and it is not uncommon to observe third and

fourth order branches on cereal roots [1,2].

Over the past decade, it has become apparent that the developmental

pathways of the different root types of cereals are at least partly distinct.

In both rice and maize, for example, crossing a crown rootless (CRL)

mutant with a primary rootless mutant produces a double mutant with

an additive phenotype (no crown roots and no primary root) [122,123].

Two classes of lateral root mutants have also been identified: the first

class affects both crown root and lateral root initiation, whereas the

second class specifically affects lateral root initiation [1,2]. Finally, the

effect of several abiotic factors on lateral root formation also supports

the existence of lateral root specific pathways [20,22,24,83,121,124,125],

some of which are being exploited to repress lateral root formation at a

predictable stage [22,24] and move the study of lateral root formation

forward in cereals [37].

First leaf

Coleop�le

Coleop�lar nodeSeed

Embryonic roots:Key:

Primary root

Seminal roots

Lateral roots

Crown roots

Postembryonic roots:

MesocotylScutellar node

TRENDS in Plant Science

Figure I. Maize seedling.

Review Trends in Plant Science August 2013, Vol. 18, No. 8

contrasts with many dicots, such as Arabidopsis, wherelateral root primordia originate exclusively from pericyclecells opposite protoxylem poles [12] with some exceptions[13]. Given the polyarch stelar organisation of cereal roots,which consists of several phloem poles alternating with thesame number of xylem poles, lateral roots appear in sev-eral longitudinal files (also referred to as ranks or rows)[14,15], the number of which is roughly proportional to thestele diameter [16].

Within each file, lateral root primordia formation fol-lows an acropetal sequence, with the youngest primordiaappearing closest to the root tip [12], often at a predictabledistance [17,18]. Few studies in maize [15,19] and wheat[20,21] have reported deviations from this strictly acrope-tal rule. However, the acropetal sequence can easily beobscured when lateral root primordia developmentallyarrest before emergence [18,22] or in rice when thick, longlateral roots arise between fine, short lateral roots [2,23].However, nothing is known about the control of inter-lateral distance in cereals, or whether the pattern is theresult of a spatial or temporal control mechanism (as inArabidopsis [18]).

Similar to the situation in Arabidopsis, lateral rootformation in cereals follows a succession of developmen-tal steps comprising initiation, growth through the cor-tex, and emergence through the epidermis. The first

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morphological events of lateral root initiation are ob-served on the proximal side of the elongation zone, forexample, at 10–15 mm from the root tip in maize [10,24]and at 15–20 mm from the root tip in wheat [11]. Twolongitudinally adjacent pericycle cells undergo asymmet-ric transverse divisions opposite a protophloem element(stage I in Figure 1). In barley, such paired divisions occursynchronously in four to six neighbouring pericycle cellfiles [11], compared with three files in Arabidopsis [25].The resulting two short cells expand radially (stage II inFigure 1) and undergo asymmetric periclinal divisions,giving rise to two inner and two outer cells, approximate-ly 21–24 mm from the maize root tip [15]. The two outerdaughter cells (in each file) then engage in a long succes-sion of anticlinal and periclinal divisions (spanningstages III–VII in Figure 1). Unlike Arabidopsis, endoder-mal cells adjacent to the dividing pericycle cells divideanticlinally just after stage III and contribute an addi-tional cell layer to the new lateral root primordium(Figure 1). Later on, few cells at the forefront of theprimordium divide synchronously and periclinally to gen-erate an inner layer of root cap initials and an outer layerof root cap cells. When the primordium has progressedhalf-way through the cortex (stage VI in Figure 1), amorphologically distinct meristematic zone and rootcap can be observed [15].

(A) (B)

(C)

Epidermis

Cortex

Endodermis

Pericycle

Stele �ssues

Xylem

Phloem

Puta�ve ini�als

Puta�ve quiescentcentre (QC)

Key:

(E)

(D)

(F) (G)

(I) (II) (III) (IV) (V) (VI) (VII)

TRENDS in Plant Science

Figure 1. Lateral root development in barley. (A) Illustration of a longitudinal section showing the typical tissue organisation of cereal roots. The number of cortex layers

that have to be penetrated by the developing meristem is much larger than in Arabidopsis. (B) Succession of morphological stages during lateral root development and

emergence (arbitrary stages). (C) Original toluidine blue stained sections used for illustrations in (B). (D) Periclinal and (E) anticlinal longitudinal sections of the growing

lateral roots. The sections show an extensive cortical region around the primordium where divisions are taking place. (F) Radial tissue organisation of cereal roots (toluidine

blue staining). (G) Illustration of the section in (F) to highlight the deformation of the cortex that occurs during lateral root penetration. (Scale bars = 50 mm).

Review Trends in Plant Science August 2013, Vol. 18, No. 8

During lateral root formation, overlying cortical andepidermal layers of the parent root are reprogrammed tofacilitate the emergence of the new organ. In maize as inArabidopsis, loosening of cortical cell walls occurs at earlystages of lateral root primordium development and involvescell wall enzyme action [15,26]. In cereals, this loosening ispreceded by divisions of the cortical cells directly overlayinglateral root primordia (Figure 1) [15,27,28]. These cells re-enter the cell cycle very early as mitotic figures are observedfrom stages II or III in barley, approximately 10–12 h afterthe first asymmetric division of the founder pericycle cells(A. Babe, unpublished). Many of the resulting small corticalcells enter H2O2-mediated cell death following the penetra-tion of the lateral root primordium (B. Orman, unpublished).Therefore, whereas separation of cell files seems to besufficient to allow the emergence of lateral root primordiathrough the three overlying endodermal, cortical, and epi-dermal cell layers in Arabidopsis, cell division and cell deathappear to be required for the penetration of the large lateralroot primordia of cereals through a much larger number ofcortical layers, and implies a profound reorganisation of theoverlying cells.

Genetic and hormonal control of lateral rootdevelopment in cerealsLateral root development in cereals is controlled by manyextrinsic (environmental) and intrinsic signals. Plant hor-mones represent key regulators of plant developmentalprocesses (reviewed in [29–31]), including lateral root ini-tiation, patterning, and emergence of lateral roots(reviewed in [8]). Besides the classical phytohormones,peptide hormones such as members of the CLE-Like/GOL-VEN family (reviewed in [32]), small molecules such asnitrite oxide [33,34], or reactive oxygen species [35] alsohave regulatory effects on different aspects of root devel-opment and branching. However, most of the knowledge onhormonal control of root branching has been acquired fromstudies using Arabidopsis or other dicot plants, and it isonly recently that efforts have been made to understandlateral root formation in monocots (reviewed in [36,37]). Inmonocots, most lateral root mutants also affect the devel-opment of crown roots, and a minor number specificallyaffect lateral root or crown root formation, revealing thatboth specific and common hormonal and developmentalpathways are involved in post-embryonic root formation in

461

CRL4 /OsGNOM1

PIN

AUX/IAA

Auxin

WOX11

CRL1/ARL1(OsLBD3-2)

Crownroot

ini�a�on

ARR

CK ARF

OsTIR1/OsABF2

Lateralroot

ini�a�on

Lateralroot

ini�a�on

OsMir393a

OsIAA11/OsIAA13

Cytokininresponse

CRL5

OsHO1

MJ NO

CO

CK

Rice Arabidopsis

GNOM1

PIN1

IAA14

Auxin

LBD16/LBD29

ARF7/ARF19

TIR1/ABF2

CK

Cellular events

Auxin accumula�onin the two founderpericycle cells and

nucleusrelocalisa�on

Cell cycle ac�va�on

Assymetric divisionof the two pericycle

founder cells andcell pa�erning

TRENDS in Plant Science

Figure 2. Gene regulatory networks controlling crown root and/or lateral root initiation in rice and lateral root initiation in Arabidopsis. The corresponding early cellular

events of root initiation in Arabidopsis are noted. Arrows represent the positive regulatory action of one element of the network on another one. Genes are denoted in black,

hormones in green, miRNA in blue, and regulatory molecules in red. A line ending with a trait represents the negative regulatory action of one element of the network on

another one. Dotted lines represent hypothetical links between two elements. Abbreviations: AFB2, auxin signalling F-box2; ARF, Auxin Response Factor; ARL, adventitious

rootless; ARR, type-a response regulator2; AUX/IAA, auxin/indole-3-acetic acid; CK, cytokinin; CO, carbon monoxide; CRL, crown rootless; GNOM1, membrane-associated

guanine nucleotide exchange factor of the ADP-ribosylation factor G protein (ARF-GEF); HO1, heme oxygenase 1; LBD, lateral organ boundaries domain; MJ, methyl

jasmonate; NO, nitric oxide; PIN, pin-formed auxin efflux carrier proteins; TIR1, transport inhibitor response 1; WOX11, WUSCHEL-Related Homeobox 11.

Review Trends in Plant Science August 2013, Vol. 18, No. 8

cereals. Because many lateral root mutants have beeninitially analysed in the context of crown root formation,parts of our review will cover both processes. An updatedschema of the regulatory pathway controlling crown rootand/or lateral root initiation in rice compared with corre-sponding steps for lateral root initiation in Arabidopsis ispresented in Figure 2.

Auxin

To date, the majority of mutants reported to be affected inlateral root and crown root initiation, patterning, and emer-gence have been auxin-related (reviewed in [1,2,38]). Auxinis a common regulator for all monocot root types. Studieshave reported a positive correlation between auxin biosyn-thesis and crown root initiation frequency in rice [39], apositive effect of auxin treatments on lateral root formationin rice, maize, and barley [22,24,27], as well as a negativeeffect of blocking auxin transport in rice and maize[24,27,40].

The differential distribution of auxin throughout thevarious root tissues and cell types is at the core of its modeof action during all developmental processes. Such distri-bution is achieved through tightly orchestrated polartransport mechanisms, which result in the local inductionof an auxin response in specific cell types at defined timepoints. Reporter constructs containing the synthetic pro-moter DR5 [41] have been instrumental in helping tovisualise local auxin responsive gene expression and haverevealed a role for auxin in lateral root initiation [42] andpatterning in Arabidopsis [43]. Similar reporters havebeen used in monocots such as rice, maize, and barley

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[27,44,45] to monitor auxin responses during lateral rootinitiation [24,27,46,47] and during crown root initiation inrice [48]. In the primary root of maize, a detailed survey ofDR5 expression at the tissue level revealed the involve-ment of auxin in vascular element differentiation, pericyclespecification, and lateral root initiation [24]. Interestingly,an auxin response maximum at the phloem poles precedesthe first divisions of the pericycle in monocots, which isreminiscent of the priming of the xylem pole pericycle cellsreported in Arabidopsis [49]. Similar observations havebeen made in rice using another auxin responsive reporteremploying the soybean GH3 promoter [27,50].

Over the past decade, several genes orthologous to theArabidopsis auxin transport/signalling cascade have beencharacterised in monocots. Although it is often unclearwhether these act in a root cell type-specific manner(Box 1) or have a more generic contribution in all root celltypes, many of the components belonging to the canonicalauxin signalling pathway involved in lateral root initiationin Arabidopsis, from transport to downstream responses,have also been identified in monocot species.

Auxin transport

Both PIN-FORMED (PIN) and AUX1 classes of auxin effluxand influx carriers are involved in lateral root formation incereals. PIN auxin efflux carriers, such as ETHYLENEINSENSITIVE ROOT (EIR) [51,52], and AUX1 influx car-riers are expressed in specific areas of the root in relation tolateral root formation, in rice [53] and barley (B. Orman,unpublished), respectively. The maize homologue of AUX1is also highly expressed during brace root initiation [54].

Review Trends in Plant Science August 2013, Vol. 18, No. 8

In Arabidopsis, the intracellular trafficking of PIN1 isregulated by GNOM1, a membrane-associated guaninenucleotide exchange factor of the ADP-ribosylation factorG protein (ARF-GEF) [55]. GNOM1 is required for the firstasymmetrical division of pairs of pericycle cells, whichtriggers lateral root initiation in Arabidopsis [8,56]. Muta-tions in the rice gene orthologous to GNOM1, crown root-less 4 (crl4) [57] and Osgnom1 [58], exhibit no crown rootsand a reduced number of lateral roots [58]. In addition, theexpression of OsPIN2, OsPIN5b, and OsPIN9 is altered inOsgnom1, indicating that polar auxin transport involvingOsPIN auxin carriers and regulated by CRL4/OsGNOM1is required for crown root and lateral root initiation in rice.

Interestingly, some monocot PIN sequences do notcluster with dicot sequences, suggesting the existence ofclade-specific pathways [52]. An extensive characterisa-tion of PIN, AUXIN1/LIKE-AUX1 (AUX/LAX), and P-GLYCOPROTEIN (PGP) classes of auxin transport pro-teins has been initiated in sorghum (Sorghum bicolor)[59,60] and suggests their involvement in root develop-ment, but a direct link with lateral root initiation has yet tobe investigated.

Auxin perception

AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) proteins arekey regulators of the nuclear auxin response pathway andseveral of them have been shown to modulate lateral rootformation in Arabidopsis [61]. These short-lived nuclearproteins function as auxin co-receptors with TRANSPORTINHIBITOR RESPONSE 1 (TIR1) and closely relatedAUXIN SIGNALLING F-BOX (AFB) proteins [62]. Aux/IAA proteins also function as transcriptional repressors byinteracting with members of the AUXIN RESPONSEFACTORS (ARF) transcription factor family. In the pres-ence of auxin, Aux/IAA proteins are degraded via ubiqui-tination by the E3 ligase Skp1–Cullin–F-box protein(SCF)TIR1/AFB complex, thereby derepressing ARF activity.Several components of this nuclear auxin response path-way have been identified in cereals that regulate lateralroot formation.

Mutations in Aux/IAA proteins such as OsIAA13 [47] inrice and ROOTLESS WITH UNDETECTABLE MERIS-TEMS 1 (RUM1) in maize [63,64] that block their auxin-mediated degradation confer lateral root defects. Therum1-R (rootless with undetectable meristems 1-Reference)mutant is deficient in polar auxin transport and lacksembryonic seminal roots and post-embryonic lateral rootsin the primary root. RUM1-R encodes a truncatedZmIAA10 sequence that lacks the auxin degron sequence.ZmIAA10 can interact with ZmARF25 and ZmARF34 [64],suggesting that an auxin–AUX/IAA-ARF pathway regu-lates lateral and seminal root initiation in maize.

The gain-of-function mutant Osiaa13 contains a singleamino acid substitution in the degron sequence requiredfor the auxin-triggered turnover of the OsIAA13 protein[47]. Osiaa13 exhibits a lateral rootless phenotype, yetcrown root initiation and development are not modified,suggesting that the stabilised OsIAA13 protein specificallyinhibits the auxin transduction pathway involved in later-al root initiation. This is also supported by the specificexpression of OsIAA13 in the pericycle and endodermis, in

regions where lateral roots are initiated [65,66]. Further-more, root transcriptome laser dissection analysis revealedthat 71 genes could be associated with lateral root initia-tion in rice, of which 21 have a functional annotation [65].Nine of these 21 genes are differentially regulated inOsiaa13 relative to the wild type [47], and seven of themcontain an auxin response element in their promotersequences that can function as binding sites for ARF. Thislist of genes includes transcription factors [67], cell wallmodification enzymes, and Cdc2 protein kinases [47]. How-ever, further analysis is required to confirm their function-al importance during lateral root initiation in rice.

OsIAA11 and OsIAA30 show sequence and expressionpattern similarities with OsIAA13 [66,68]. Interestinglythe gain-of-function mutant Osiaa11 also has a lateral rootdefect [46], suggesting that OsIAA11, OsIAA13, and per-haps OsIAA30 have redundant functions controlling later-al root initiation in rice.

Other components of the auxin response pathway havealso been shown to control lateral root development incereals. In rice, mutations in Cyclophilin 2 (OsCYP2)and Cullin-associated Nedd8-dissociated protein 1(OsCAND1), which are involved in the assembly of theE3 ubiquitin ligase SCFTIR1/AFB complex, cause the cellcycle to arrest at the G2/M transition, resulting in defectsin lateral root initiation [69] and crown root emergence[70], respectively.

miRNAs OsMir393a and OsMir393b, negative regula-tors of the messenger RNAs OsTIR1 and OsAFB2, the riceorthologues of Arabidopsis auxin co-receptors TIR1 andAFB2 [71,72], also appear to be involved in lateral rootinitiation in rice. Overexpression of 35S::Mir393 leads to areduced number of crown roots and a strong auxin-resis-tant phenotype [71]. The GUS reporter gene controlled bythe OsMir393a promoter sequence is expressed in thecrown root and at lateral root initiation sites. GUS stainingaccumulates transiently in the pericycle cells during theearly stages of lateral root formation, suggesting thatOsMir393a may be involved in a feedback regulatory loopof auxin signalling during lateral root initiation.

Auxin response

Aux/IAA protein degradation releases ARF transcriptionfactors, thereby activating a set of downstream targetgenes, including LATERAL ORGAN BOUNDARIES DO-MAIN (LBD) proteins. In Arabidopsis, the positive regu-lation of LBD16 and LBD19 by ARF7 and ARF19 isessential for lateral root initiation and occurs just afterauxin perception by TIR1/ABF auxin receptors that me-diate the degradation of Aux/IAA [73–76]. In rice,OsARF16, the orthologue of ARF7 and ARF19 in Arabi-dopsis, binds auxin response elements located in theCROWN ROOTLESS 1 (CRL1) promoter [48]. CRL1encodes OsLBD3-2, which is closely related to LBD16and LBD19 in Arabidopsis [67]. Two mutants ofOsLBD3-2, crl1 [48] and adventitious rootless 1 (arl1)[77], are devoid of crown roots and present a reducednumber of lateral roots (70% reduction in crl1 comparedwith the wild type). The induction of CRL1 expression byauxin is disrupted in plants overexpressing an ubiquitin-insensitive mutated AUX/IAA protein. A comparative

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Review Trends in Plant Science August 2013, Vol. 18, No. 8

transcriptome analysis of crl1 versus wild type stem basesrevealed the existence of CRL1-dependent auxin-regulat-ed genes but further functional analysis is required todetermine if these are downstream targets of CRL1 in-volved in crown and lateral root initiation [78].

In maize, mutations in LBD proteins such as ROOT-LESS CONCERNING CROWN AND SEMINAL ROOTS(RTCS) [79], orthologous to the rice gene ARL1/CRL1,interfere with the initiation of crown and seminal, but notlateral roots [80,81]. RTCS and its duplicated homologousgene RTCS-LIKE (RTCL) could share functional redun-dancy and coregulate lateral root initiation [79]. RTCSand RTCL can form heterodimers and bind to an LBDmotif present in the promoter of ZmARF34. In turn,ZmARF34 binds with the auxin response elements pres-ent in RTCS and RTCL promoters [82]. In maize, inor-ganic phosphate (Pi) starvation was exploited toexperimentally interfere with lateral root initiation anda gene expression study comparing the lateral root initi-ation zone of the seminal root of plantlets cultivated withor without Pi revealed that ZmLBD17 and several genesencoding auxin biosynthesis enzymes or involved in auxintransport were found to be upregulated in response to Pideprivation [83].

Cytokinins

Cytokinin and auxin have antagonistic effects on rootdevelopment in Arabidopsis. In particular, cytokinins dis-rupt lateral root formation and patterning by influencingauxin transport and homeostasis [8,84–86]. In rice, treat-ment with cytokinin or an inhibitor of cytokinin oxidase(CPPU) leads to inhibition of lateral and crown root initia-tion and stimulation of lateral root elongation [87,88].Inhibiting the cytokinin signalling pathway by downregu-lation of type-A RESPONSE REGULATORS (OsRR2 andOsRR1) known to function as repressors of cytokinin sig-nalling [89,90] also leads to a reduction in crown rootinitiation, as shown in the mutants wuschel-related homeo-box 11 (wox11) [91] and crl5 [47,88]. However, crl5 does notimpair lateral root initiation, suggesting that a differentgenetic pathway is involved in regulating lateral rootinitiation by cytokinin.

Jasmonic acid, nitric oxide, and carbon monoxide

signals

Jasmonic acid has been proposed to act independently ofauxin to induce lateral roots in rice [92]. Methyl jasmo-nate, nitric oxide, and auxin induce lateral root initiationin rice and it is hypothesised that this occurs via theinduction of HEME OXYGENASE 1 (OsHO1) expression,through a calcium- and calmodulin-dependent signaltransduction pathway [34,93]. OsHO1 can produce carbonmonoxide, a molecule known to promote lateral root initi-ation in different species. A similar pathway exists inmaize and the overexpression of ZmHO1 in Arabidopsisimpacts on the expression of different Arabidopsis cyclin-dependent kinases involved in lateral root initiation [94].This suggests that HO1 genes and carbon monoxide pro-duction may constitute a key relay in the promotion oflateral root initiation by different signals and hormones inmonocots.

464

Ethylene

As yet, there is only limited knowledge about the role of thegaseous hormone ethylene during the formation of lateralroots in monocots. In Arabidopsis, ethylene has beenreported to inhibit lateral root formation because ethyl-ene-insensitive mutants form more lateral roots [95,96].The downregulation of ETHYLENE-INSENSITIVE 3(EIN3) transcription (a key transcription factor promotingethylene regulated gene expression) during maize braceroot initiation may indicate a role for this pathway inmonocots [54]. By contrast, stimulation of crown rootemergence by ethylene in deep water rice upon floodingis much better studied (reviewed in [97,98]). In these roots,ethylene promotes the growth of the primordium [40,99]and the breakdown of surrounding epidermal cell layers[40,99,100]. In addition, crown root emergence is facilitat-ed by H2O2-mediated cell death, weakening the epidermalcell barrier [100–102]. This role of ethylene is not exclusiveto monocots because it has also been shown to promote thegrowth of adventitious roots in other dicotyledonous spe-cies [103] and insensitivity to ethylene has been shown toresult in slower growth of adventitious roots [104].

Concluding remarks and future perspectivesEvolutionary considerations about post-embryonic root

formation

Although the whole Arabidopsis post-embryonic formationprogramme cannot be directly translated to cereals, somelevel of conservation has been maintained since the mono-cot–dicot divide, which should help to orient and to accel-erate cereal root research. However, several fundamentalquestions about the evolution of post-embryonic formationin plants remain.

Similar to Arabidopsis, the auxin–TIR1/ABF2–AUX/IAA-ARF–LBD pathway is involved in post-embryonic rootinitiation in rice and maize, suggesting that this corepathway must have been recruited at an early stage intheir evolutionary history before the differentiation ofmonocots and dicots [67]. Most crl mutants related to thispathway also present a significantly reduced number oflateral roots (crl1, crl4), whereas some mutants are spe-cifically affected in lateral root initiation (Osiaa11 andOsiaa13). This raises the question of the occurrence of acommon ancestral mechanism governing post-embryonicroot formation in the primitive, undifferentiated axis(telome) of early land plants that may have evolved differ-ently in stem and in roots.

In rice, crown roots initiate from the ground meristemlocated between the centre of the stem containing thevascular tissue and the starch granule rich cell layers thatconstitute the shoot endodermis [105,106]. The existence ofa pericycle-like tissue layer in the shoot has been suggestedin Arabidopsis [107] and it is tempting to propose that theground meristem in rice represents such a tissue. Furthercomparative studies of the histological and molecularmechanisms involved in crown root and lateral root initia-tion in monocots and dicots should give a better under-standing of the evolution of genetic pathways controllingpost-embryonic root development. The recruitment of theendodermis to the lateral root formation process in cerealsand the fact that initiation can occur in front of protoxylem

Review Trends in Plant Science August 2013, Vol. 18, No. 8

or protophloem depending on the species are still intrigu-ing questions that need to be further investigated.

Future lines of research

The increasing availability of next generation sequencing(NGS) techniques should greatly facilitate comparativedevelopmental approaches in dicots and monocots anduncover conserved signalling mechanisms. For example,NGS may help in the discovery of novel roles for new andexisting hormones during lateral root primordial develop-ment in the near future. For instance, the conservation ofexpression patterns by members of the gibberellin-regu-lated transcript GAST gene family that are expressed inlateral root primordia in dicots [108,109] and monocots[110] may indicate a potential role for gibberellic acidduring root development. Similarly, strigolactones, absci-sic acid, and brassinosteroids, which play a role in lateralroot formation in Arabidopsis, are also present in monocotspecies but their potential action on root formation has notyet been investigated. In addition to the classic hormones,a role for the CLE-Like/GOLVEN signalling peptide familyhas recently been deciphered in relation to lateral rootinitiation in Arabidopsis [111]. These peptides are alsopresent in rice but their functions are unknown [112].

Since the sequencing of its genome, many mutantresources have been created in rice [113–115]. Screeningthese mutant collections for root development defects hasenabled researchers to identify known genes involved inlateral root initiation. Other mutants affected in lateralroot development have been described but the correspond-ing genes have not been isolated [1]. As most of thesemutants also present an auxin-resistant phenotype, it islikely that their functional characterisation will providenew information to better understand the auxin-relatedlateral root initiation gene regulatory pathway.

Cereals possess several different types of post-embry-onic roots, emphasising that studies of root organogenesiscannot be addressed solely by using Arabidopsis as a modelspecies. The majority of the described cereal mutantsaffected in lateral root formation refer to primary (embry-onic) roots [63], so one cannot also exclude the possibilitythat the mechanism(s) of lateral root formation would bedifferent for primary compared to crown roots [37,81].

Lateral roots for the second green revolution

Domestication and selection of cereals started 10 000 yearsago, resulting in the creation of several genetic resourcesadapted to a wide range of climatic and soil conditions. Thisevolution has gone beyond allelic frequency changes, asexemplified by the loss of Pstol1, a gene conferring toleranceto low phosphorus that was present in a traditional ricevariety [116]. This genetic diversity, which is particularlylarge in cereal crops, is likely to be a unique resource fordiscovering novel adaptive root development mechanismsthat support productivity under suboptimal conditions.

After two decades of mapping root-related quantitativetrait loci (QTLs) using biparental mapping populations[117], association mapping using natural populations com-prising hundreds of varieties has become the most prom-ising way to explore cereal biodiversity [118]. As it is nowrelatively easy to genotype large numbers of lines, the next

rate-limiting step will be the development of high-through-put root phenotyping systems under laboratory or fieldconditions. Progress in this area will become increasinglyimportant as we attempt to bridge the genotype to pheno-type gap and identify the key genes and processes thatcontrol root architecture to accelerate the development ofimproved cereal varieties.

To date, evidence that lateral root traits have been usedsuccessfully in cereal breeding to enhance resource captureremains scanty [119]. A recent assessment on the contri-bution of root traits for a second green revolution suggeststhat lateral root formation and growth might be importanttargets in maize and presumably other cereals [120]. As amore detailed understanding of the regulatory mecha-nisms controlling post-embryonic root development isgained, we move closer to the ability to predictively designa root system optimised to enhance and maximise cropperformance through resource capture.

AcknowledgementsWe thank the FWO (Flanders Research Foundation, project G0273.13N),the FRIA (Fonds pour la Recherche dans l’Agriculture et l’Industrie)fellowship to B.O., BBSRC (Biotechnology and Biological SciencesResearch Council) funding to M.J.B., the Belgian Science Policy Office(grant IAP7/29) to B.P., T.B., M.J.B., and X.D., and the Communautefrancaise de Belgique (Actions de Recherche Concertees, grant 11/16-036).

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