Comptes Rendus

Plant biology and pathology/Biologie et pathologie végétales
Plant development: A TALE story
Comptes Rendus. Biologies, Volume 333 (2010) no. 4, pp. 371-381.


Plant development depends on the activity of a group of dividing cells called the meristem. Extensive genetic analyses have identified the major regulators of the shoot apical meristem (SAM), which control the development of all aerial organs. Among them, the three-amino-acid-loop-extension (TALE) class of homeoproteins has been shown to control meristem formation and/or maintenance, organ morphogenesis, organ position, and several aspects of the reproductive phase. This family contains the KNOTTED-like homeodomain (KNOX) and BEL1-like Homeodomain (BELL) members, which function as heterodimers. In this review, we have reported the functions of the TALE members throughout the Arabidopsis life cycle. Genetic analyses revealed a complex network, as TALE members exhibit both overlapping and antagonistic activities. The characterization of a new KNOX member (KNATM), which lacks a homeodomain and interacts with other members to modulate their activities, adds another layer of complexity to this network. While the mode of action of these transcription factors is still largely unknown, they have been implicated in the regulation of several hormonal pathways, providing a link between gene regulatory networks and signaling in the SAM.

Le développement des plantes dépend de l’activité de petits groupes de cellules en division : les méristèmes. Les analyses génétiques réalisées chez Arabidopsis ont permis d’identifier les régulateurs majeurs du méristème apical caulinaire. Parmi ceux-ci, la famille de facteurs de transcription à homéodomaine TALE joue un rôle critique puisque ses membres régulent l’initiation et le maintien du méristème, la forme et la position des organes, et plusieurs aspects de la phase reproductrice. Cette famille comprend les membres KNOX et BELL qui sont actifs en tant qu’hétérodimères. Dans cette revue, les fonctions des protéines TALE au cours du cycle d’Arabidopsis sont présentées. Les analyses génétiques ont permis de révéler une fonction pour la moitié des membres de cette famille. Le réseau TALE est complexe, car ses membres ont des fonctions à la fois redondantes et antagonistes. La caractérisation d’un nouveau membre KNATM qui a perdu l’homéodomaine, mais qui peut néanmoins interagir avec les autres membres et moduler leur activité vient ajouter une nouvelle dimension à cette complexité. Bien que le mode d’action de ces facteurs de transcription soit encore mal connu, ils ont été impliqués dans la régulation de plusieurs voies de signalisation hormonale, fournissant ainsi un lien entre le réseau d’interaction génétique et la signalisation dans le méristème.

Published online:
DOI: 10.1016/j.crvi.2010.01.015
Keywords: KNOX, BELL, Homeodomain, Shoot apical meristem, Organogenesis
Mot clés : KNOX, BELL, Homéodomaine, Meristème apical caulinaire, Organogenèse

Olivier Hamant 1; Véronique Pautot 2

1 Laboratoire de reproduction et développement des plantes, INRA, CNRS, ENS, université de Lyon, 46, Allée d’Italie, 69364 Lyon cedex 07, France
2 INRA, institut Jean-Pierre-Bourgin, route de St-Cyr, 78026 Versailles cedex, France
     author = {Olivier Hamant and V\'eronique Pautot},
     title = {Plant development: {A} {TALE} story},
     journal = {Comptes Rendus. Biologies},
     pages = {371--381},
     publisher = {Elsevier},
     volume = {333},
     number = {4},
     year = {2010},
     doi = {10.1016/j.crvi.2010.01.015},
     language = {en},
AU  - Olivier Hamant
AU  - Véronique Pautot
TI  - Plant development: A TALE story
JO  - Comptes Rendus. Biologies
PY  - 2010
SP  - 371
EP  - 381
VL  - 333
IS  - 4
PB  - Elsevier
DO  - 10.1016/j.crvi.2010.01.015
LA  - en
ID  - CRBIOL_2010__333_4_371_0
ER  - 
%0 Journal Article
%A Olivier Hamant
%A Véronique Pautot
%T Plant development: A TALE story
%J Comptes Rendus. Biologies
%D 2010
%P 371-381
%V 333
%N 4
%I Elsevier
%R 10.1016/j.crvi.2010.01.015
%G en
%F CRBIOL_2010__333_4_371_0
Olivier Hamant; Véronique Pautot. Plant development: A TALE story. Comptes Rendus. Biologies, Volume 333 (2010) no. 4, pp. 371-381. doi : 10.1016/j.crvi.2010.01.015. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.1016/j.crvi.2010.01.015/

Version originale du texte intégral

1 Introduction

In the development field, homeosis certainly is one of the most spectacular effects that a mutation can cause: in homeotic mutants, at a given position, the identity of an entire organ is replaced by that of another organ. These phenotypes, which had been noticed by botanists since antiquity, were explained in animals by the misexpression of conserved transcription factors, called homeoproteins, exhibiting a common helix-turn-helix DNA binding domain, the homeodomain. Homologs in plants were identified [1–3]. While the role of the plant homeoproteins in homeosis turned out to be rather scarce, this family of ca. 105 members in Arabidopsis contains among the most crucial effectors of plant development. In this review, we will focus on a particular class of homeoproteins, the three-amino-acid-loop-extension (TALE) homeoproteins, which contain a three-amino acid extension in the loop connecting the first and second helices of their homeodomain [4–6].

The plant TALE homeodomain superclass comprises the KNOTTED-like homeodomain (KNOX) and BEL1-like homeodomain (BELL) proteins that are structurally and functionally related (Fig. 1). As observed for the animal TALE homeoproteins MEIS (including vertebrate Meis and Prep, fly Homothorax (Hth) and worm Unc-62) and PBC families (vertebrate Pbx protein, fly Extradenticle Exd and worm Ceh-20), the KNOX and BELL proteins function as heterodimers and have evolved a complex regulatory mechanism controlling their subcellular localization (Box 1).

Fig. 1

The TALE proteins: dissecting their sequences. A. Phylogeny of the TALE superfamily. B. Schematic structures of the KNAT and BELL proteins; KNAT proteins contain a MEINOX (from MEIS “Myeloid ecotropic viral integration site” and KNOX) domain composed of two subdomains, KNOX1 and KNOX2, separated by a flexible linker, an ELK domain and a TALE homedomain which has three-extra-amino-acids (Proline [P]-tyrosine [Y]-Proline [P]) between the first and the second helix. The MEINOX domain mediates interactions with other KNOX and TALE proteins. The KNATM protein has no homeodomain. KNATM interacts with BELL proteins through the MEINOX domain and interacts with BP via the BPID (BP interacting domain). BELL proteins contain a TALE homeodomain, a MID (MEINOX interacting domain) composed of the SKY and BELL regions. The BELL domain harbors two nuclear exclusion leucine-rich sequences (NES) involved in the interaction with KNOX proteins and with the nuclear export receptor atCRM1.

Genetic and molecular analyses have revealed overlapping and distinct functions for the TALE proteins during plant development. In this review we aim at precisely dissecting these functions during the main steps of the plant post-embryonic life. For this purpose, we will mostly focus our survey on data from Arabidopsis, and in some specific cases from other species.

2 TALE proteins control the establishment and maintenance of the shoot apical meristem

Shoot apical meristems (SAM) are populations of dividing undifferentiated cells that generate lateral organs at the apices of stems and branches throughout the life of a plant (for a detailed review on the SAM, see [7–10]). As it balances two opposing functions, organ production and self-maintenance, the SAM is one of the most dynamic structures in biology. In the past two decades, developmental biologists have turned to molecular genetics to determine the molecular basis of SAM functions and identified keys effectors involved in transcriptional regulation and hormonal signaling, the TALE proteins having a major position in this framework.

2.1 TALE proteins display various levels of contribution to meristem establishment and maintenance

In Arabidopsis, the KNOX family is divided in three classes (Fig. 1): class I KNOX genes are mainly expressed in the meristematic tissues, and include SHOOTMERISTEMLESS (STM), BREVIPEDICELLUS (BP)/KNAT1, KNAT2 and KNAT6. Class II KNOX genes are broadly expressed and comprise KNAT3, KNAT4, KNAT5 and KNAT7. Class III contains a unique member, KNATM, which produces three isoforms by alternative splicing [11]. KNATM is expressed in the organ primordia and at the boundary of mature organs and is excluded from the SAM. In contrast to other KNAT genes, KNATM is found only in dicots [11]. KNATM protein has no homeodomain, but interacts with BELL proteins through its MEINOX domain and dimerizes with BP through an acidic coiled-coil domain named BP-interacting domain (BPID) ([11] and Box 1). Thus, KNATM may regulate transcription independently of the homeodomain through the titration of other TALE proteins or as a transcriptional cofactor [11].

The BELL family comprises 13 members (Fig. 1, Table 1 and Box 1). So far a function has only been proposed for BELL1 (BEL1) the founder of the family, PENNYWISE (PNY), also known as BELLRINGER (BRL), REPLUMLESS (RPL), VAAMANA (VAN) or LARSON (LSN), POUND-FOOLISH (PNF) a close relative of PNY, SAWTOOTH1 (SAW1), SAW2 and ARABIDOPSIS HOMEOBOX 1 (ATH1) [12–22].

Table 1

TALE genes expression.

Gene name Accession Number Expression pattern Refs.
STM At1g62360 Embryo, SAM, IM, axillary meristems, FM, carpel [16,25,124]
BP/KNAT1 At4g08150 SAM, IM, stem (cortex), pedicel, style, base of lateral roots [13,113,125,126]
KNAT2 At1g70510 Embryo, root, SAM, FM, and carpel [30,36,61,93,127]
KNAT6 At1g23380 Embryo, root, SAM, FM, flower, and carpel [30,93,128]
KNAT3 At5g25220 Expressed in most tissues. In elongated zone of the mature root (pericycle, endodermal and cortical cells) [111,113]
KNAT4 At5g11060 Almost every organ. Root (phloem, pericycle cells and endodermis). [111,113]
KNAT5 At4g32040 Almost every organ. Elongation and differenciation zones of the main root (epidermis) [111,113]
KNAT7 At1g62990 Xylem [110]
KNATM At1g146760 Organ primordia, leaves and FM [11]
BEL1 At5g41410 Integument of ovule, IM and FM, leaves, sepals [12,19,121]
ATH1 At4g32980 SAM, young leaves, flowers: stamens, carpels [20,21,129]
BLH1 At2g35940 Transmitting track and funiculus, [108]
BLH2/SAW1 At4g36870 Leaves, sepals, petals, anther filament, style, transmitting track, stem [19]
BLH3 At1g75410 IM FM [31]
BLH4/SAW2 At2g23760 Cotyledons, leaves, sepals, anther filament, style, transmitting track, stem [19]
BLH5 At2g27220 Unknown
BLH6 At4g34610 Embryo, IM, flowers: anthers, stigma [130]
BLH7 At2g16400 Unknown
BLH8/PNF At2g27990 SAM, IM, FM [13,14]
BLH9/PNY/BLR/RPL/VAN/LSN At5g02030 SAM, IM, FM, stem, replum [13–16]
BLH10 At1g19700 Unknown
BLH11 At1g75430 Unknown

Strong alleles of stm mutants fail to form a meristem and to produce lateral organs. Based on this phenotype, a role for STM in meristem initiation during zygotic embryogenesis, and maintenance during the post-germinative growth has been proposed [23–25]. Consistent with these genetic data, STM is expressed in the SAM, except in the initium, the site where a new organ is initiated. The ortholog of STM in maize, KNOTTED1 (KN1), is the founder of the KNOX subfamily and when disrupted also leads to defects in meristem maintenance [26–28].

The role of four other TALE genes, namely BP, PNY, KNAT6 and ATH1 in SAM initiation and maintenance has also been demonstrated by the observation that their inactivation aggravates the weak stm allele phenotypes [13,14,16,22,29,30]. The contribution of PNF to the SAM function is only found in the absence of PNY or both PNY and ATH1 and is likely due to the fact the STM protein requires these factors to become nuclear [22,31].

2.2 Dissecting the contributions of Class I KNOX genes in the different domains of the SAM

Due to its pattern, STM has become a marker of meristematic cell identity. Within the SAM, three subdomains, all expressing STM, can be distinguished based on histological, genetic and functional features (for a review, see [7,9,10]). First, the central zone, with CLAVATA 3 (CLV3) as a genetic landmark, contains the population of slowly dividing stem cells of the meristem. The peripheral zone surrounds the central zone and, thanks to a higher rate of proliferation, provides the cells required for lateral organ formation. In the tornado2 (trn2) mutant, the STM expression domain is increased but the markers of the central zone are not affected, suggesting that TRN2 specifically regulates the meristematic identity in the peripheral zone, thus uncoupling STM functions in both domains [32]. TRN2 encodes a tetraspanin-like membrane protein, a family of proteins that has been shown to contribute to signal transduction in animals. A similar function in plants is supported by the fact that TRN1, a Leucine-rich repeat protein, belongs to the TRN2 pathways as well [33].

Last, the third subdomain of the meristem is the boundary, a domain that separates the meristem sensu stricto from the growing primordium, and which can be spatially defined by the pattern of the CUP-SHAPED COTYLEDON (CUC) mRNA. There is accumulating evidence suggesting that this domain contains cells that promote meristematic identity, while undergoing major morphogenetic changes. In particular, the CUC proteins activate the expression of STM as well as other class I KNOX genes and repress growth in the boundary of organ primordia to allow organ separation [30,34]. Consistent with this, double mutants in two of the three CUC genes exhibit cotyledon fusions and stm strong alleles display a fusion of the cotyledon petioles, thus revealing defects in organ separation from the meristem [24]. A contribution of PNY, KNAT6, ATH1 and PNF in organ separation has also been shown [18,21,22,30]. Conversely, the ectopic expression of class I KNOX genes extends the undifferentiated state of the cells beyond the meristematic domain [35,36].

2.3 A mechanism: TALE proteins regulate hormonal pathways to maintain meristematic cells in an undifferentiated state

The redundant function of the KNOX proteins in meristematic cell maintenance has been correlated to their shared function in controlling the homeostasis of cytokinins (CKs) and gibberellins (GAs) (for a review, see [37]). CKs are plant hormones involved in cell proliferation while GAs notably control leaf morphogenesis [38–41]. The activation of KNOX proteins leads to an increase of CK biosynthesis by up-regulating the accumulation of AtIPT7 mRNA levels, and to the activation of a type-A ARABIDOPSIS RESPONSE REGULATOR 5 (ARR5), a CK response factor. Conversely, plants overproducing CKs have higher levels of BP/KNAT1 and STM mRNAs and can rescue the stm mutant [42–45].

In addition to their impact on CKs, KNOX proteins have been shown to negatively regulate GA biosynthesis through direct transcriptional repression of the GA-biosynthesis gene GA 20-oxidase [46–48]. Consistent with these data, exogenous GA partially suppressed the phenotype induced by KN1 and KNAT1 overexpression ([47], see next sections). Conversely, the stm phenotype was enhanced in the constitutive GA signaling mutant spindly. Furthermore, both KNOX proteins and CKs activate a GA-2 oxidase gene triggering GA catabolism, thereby excluding GAs from the SAM [43]. Thus, the maintenance of the SAM by KNOX proteins involves the regulation of both CKs and GAs pathways.

In addition to the crosstalks between TALE and CKs or GAs, SAM maintenance relies on a complex network involving other regulators of stem cell and hormone signaling as well. For instance, the stem cell maintenance involves a network with several feedback loops where CK plays a central role. CKs simultaneously activate the homeodomaine protein WUSCHEL (WUS) and repress CLV1 [49] [50]. Besides, the disruption of a type A ARR, a negative response regulator of CKs, in the maize aberrant phyllotaxy 1 (abph1) mutant leads to an enlarged meristem, a phenotype which could be associated with increased KN1 expression levels, at least in the embryo [51,52]. Interestingly, ABPH1 has also been shown to act as a positive regulator of PINFORMED (PIN) expression and auxin levels [53]. This is consistent with the phyllotactic defects observed in the abph1 mutant (see next sections for a discussion on auxin and phyllotaxis). To summarize, while the crosstalks between the TALE and CKs and GAs play a crucial in SAM maintenance, further work is required to integrate other factors, like WUS and auxin, in this network.

3 Downregulating TALE expression at sites of organ initiation

KNOX proteins are crucial to maintain a population of undifferentiated cells in the SAM and thus to prevent cells from being recruited too early in the primordium. In the initium, the KNOX genes are repressed to allow the exit of organ founder cells from the SAM. Organ emergence is then associated with an increased growth rate and cell expansion. Several hormones, including GA, ethylene and auxin have been shown to control these responses [37,54].

Recent evidence suggests that auxin may play a major role in downregulating KNOX genes during organ emergence. The auxin transport inhibitor naphthylphthalamic acid (NPA) induces KNOX ectopic accumulation in maize leaf primordia [55]. Disruption of auxin efflux in the pin1 pinoid double mutant also de-repressed STM expression [56]. Interestingly, the defects in leaf formation in mutant in auxin transport (pin-formed1 (pin1) or auxin signaling (axr1) were enhanced in pin as1 or axr1 as1 double mutants and were associated with the ectopic expression of BP. The reduction in leaf number of the pin1 mutant was partially rescued by BP inactivation, suggesting that the auxin dependent repression of KNOX genes is required for primordium formation [57]. It is not known whether the KNOX downregulation in the incipient primordium is maintained in these mutants. The finding of a correlation between auxin maxima and the initial downregulation of KNOX genes in the incipient leaf primordium suggests that this is the case [58,59], but further genetic analyses are required to demonstrate this conclusively. The JAGGED LATERAL ORGAN (JL0) protein, which is required to maintain the boundary domain, may play a central role as it coordinates KNOX and PIN activity [60].

Ethylene may be involved in regulating SAM activity since an antagonistic interaction between KNAT2 and ethylene has also been reported [61]. The domain of KNAT2 expression was restricted in the presence of ethylene and in the constitutive triple response 1 (ctr1) mutant, but enlarged in the ethylene insensitive mutant ethylene response 1 (etr1). The KNAT2 overexpressor phenotype was partially rescued by the application of an exogenous ethylene precursor and in the ctr1 mutant. Conversely, overexpression of KNAT2 increased the number of cells in the SAM of ctr1 [61].

To conclude, several clues point to a hormone-dependent downregulation of KNOX genes in the incipient primordium. The identity of the genetic factors responsible for this control is still unknown.

4 TALE expression shapes the leaf

4.1 KNOX expression is regulated during leaf growth

In Arabidopsis, the expression of class I KNOX genes is not detected in growing leaves and their ectopic expression leads to abnormal leaf morphologies, such as patterning defects and pronounced lobes [2,62]. Several regulators have been shown to maintain the repressed state of the class I KNOX genes in the Arabidopsis leaf. These regulators are presented below. Importantly, they are specifically involved in controlling KNOX expression after the leaf has emerged; none of them repress the KNOX genes in the incipient primordium.

Screens for mutants resembling KNOX overexpressors have led to the identification of ASYMMETRIC LEAVES 1 (AS1), a MYB transcription factor, and AS2, a member of the lateral organ boundaries-domain (LOB) protein family, which specifies adaxial fate. AS1 and AS2 down-regulate the class I KNOX genes but not STM in leaves and conversely, STM represses AS1 expression in the SAM [63,64]. Enhancers of as2 have been isolated and found to encode two key regulators of gene silencing: RNA-dependent RNA Polymerase 6 (RDR6) and ARGONAUTE 1 (AGO1). Rdr6 as1 and rdr6 as2 double mutants produce more lobed leaves, a phenotype, which is associated with the ectopic expression of BP and an increase of miRNA 165/166 levels [65]. These miRNAs regulate class III HD-Zip mRNAs that contribute to adaxial-abaxial leaf polarity. SERRATE, a zinc finger protein that regulates expression of the HD-Zip III gene PHABULOSA (PHB) via a microRNA (miRNA) gene-silencing pathway, and PICKLE, a chromatin-remodeling enzyme, seem to limit the ability to respond to KNOX activity in leaves [66,67]. Similarly, ago1 as2 double mutants display more lobed leaves and exhibit ectopic expression of all class I KNOX genes [68]. These results show that the AS1 AS2 pathway, together with RDR6 and AGO1, repress KNOX genes in leaves. Genes involved in abaxial organ identity, such as the YABBY genes, also repress KNOX class I genes, including STM, on the abaxial sides of leaves [69].

A genetic analysis identified two regulators that specifically repress the expression of the class I KNOX genes in the proximal region of the leaves: the BLADE ON PETIOLE1 (BOP1) and BOP2 genes encode proteins with ankyrin repeats and a BTB/POZ domain. They are expressed in the proximal domain of lateral organs, where they repress the BP/KNAT1 KNAT2 and KNAT6 genes [70–72].

Last, the SAWTOOTH1 (SAW1) and SAW2 proteins, two other BELL members act antagonistically to BP, KNAT6 and STM in the leaf to regulate leaf margin shape ([19], see next section).

The repression of the KNOX genes involves the chromatin state: a model suggests that AS1/AS2 complexes bind to two distinct sites of the BP promoter, create a DNA loop between the two binding sites and recruit the chromatin-remodeling protein HIRA to maintain the chromatin in a stable repressive state [65,73]. Furthermore, the Polycomb-Groups proteins CURLY LEAF (CLF) and FERTILISATION-INDEPENDENT ENDOSPERM (FIE) maintain the repressed state of KNOX genes in leaves by catalyzing the dispersed trimethylation of histone H3 at Lysine 27 (H3K27) and subsequently inducing chromatin compression and inhibition of transcription [74–76].

4.2 De-repression of KNOX genes in the leaf, or how to make leaflets

Leaf shape, and notably the formation of leaflets, is controlled by various pathways (see, for reviews, [77], Hasson et al. in this issue, and [78]). The presence of lobed leaves in KNOX overexpressor lines has suggested an important role of these genes in the formation of compound leaves [2,62]. A study of KNOX class I genes expression in various vascular plants revealed a correlation between KNOX expression and leaf shape [79]. As in species with simple leaves, KNOX class I genes are downregulated at the sites of leaf primordium initiation in the compound leaves, but are subsequently reactivated in the leaves to promote the formation of leaflets. The molecular control of leaflet formation in compound leaves seems very close to that of organ initiation at the periphery of the SAM. The molecular basis of leaflet initiation was investigated in more detail in Cardamine hirsuta (C. hirsuta), a wild relative of Arabidopsis with dissected leaves [80]. Similar to the leaf initiation at the SAM, the lateral formation of leaflets requires STM activity, which delays cellular differentiation, and the auxin efflux carrier PIN1, which generates local auxin maxima to promote leaflet formation [81]. Promoter-swap experiments indicated that the differences in BP and STM expression between Arabidopsis and C. hirsuta were associated with differences in promoter cis regulatory sequences [80]. More generally, the current model for the molecular basis of compound leaves is the presence of a cis regulatory polymorphism that would generate the diversity of the leaf morphology [73]. A cis regulatory sequence called the K-box, which is involved in the downregulation of STM in developing leaves but not in emerging primordia in Arabidopsis, has been identified in both monocots and dicots [82]. In this framework, however, the K-box most probably has a minor role in dissecting leaves in Cardamine, since it is present in both Arabidopsis and Cardamine [82].

The recent discovery of the new KNOTTED member, KNATM, in Arabidopsis and its homolog PETROSELINUM (PTS) in the tomato, has revealed an additional mechanism to regulate leaf margins [11,83]. In Arabidopsis, the two BELL members SAW1 and SAW2 redundantly repress BP, KNAT6 and STM in the leaf [19]. KNATM, which is also expressed in the hydathodes acts antagonistically to SAW1 and SAW2 as its overexpression mimics the saw1 saw2 increased leaf serration phenotype [11,19]. Because it interacts with SAW proteins, KNATM has been proposed to modulate SAW1 and SAW2 activity by titration [11]. Studies on different accessions of tomato from the Galapagos Islands, which exhibit variation in leaf shape, showed that the level of PTS correlates with leaflet formation [83]. The PTS protein binds to BIP (the SAW tomato ortholog) and thus inhibits both its nuclear localization and its interaction with leT6 (the STM ortholog of tomato). Thus high levels of PTS lead to an increase of the tomato KNOTTED1 TKN1 (the tomato BP ortholog) gene expression and renders LeT6 available to modulate leaf shape on its own or via the interaction with another partner.

To summarize, an intricate network of factors involved in transcriptional patterning, silencing and chromatin state regulates the expression of KNOX genes in the growing leaf. Together with other factors they control leaf morphogenesis and more specifically, leaflet formation.

5 TALE proteins control plant architecture

Organ emergence is a process that is integrated at the level of the whole plant. In particular, the emergence of an organ at a given position impacts the position of the following organs. This generates a pattern along the stem, which is called phyllotaxis. Several models involving a feedback loop between auxin and PIN1 localization are consistent with phyllotaxis emerging from a local cell-based response to auxin concentration or flux [58,59,84–86]. As shown earlier the link between auxin and the TALE proteins appears rather indirect. Because STM or KN1 are downregulated at the sites of incipient primordium, their expression pattern predicts the position of the organs in the SAM, and thus the phyllotaxis [87]. However, knowing the major impact of STM or KN1 disruption on the SAM itself, it remains difficult to infer a function in phyllotaxis from the mutant phenotypes only.

It must be noted that phyllotaxis not only results from the pattern initiated in the SAM, but also from the subsequent growth during stem development [88,89]. In this respect, while the SAM structure of the pny and bp mutants appears normal, major phyllotactic defects are observed in these mutants [13,14] (Peaucelle, personal communication). Notably, the pny mutants display internodes with irregular sizes and clusters of organs and bp mutants exhibit reduced internode lengths [13,14,90,91]. Mechanistically, BP regulates lignin deposition during internode development to prevent cambium-derived cells from differentiating into lignified xylem tissue. This further confirms the patterning role of this gene during the post-meristematic phase [13,90–92].

In addition, removal of KNAT6 activity suppresses the pny phenotype and partially rescues the bp phenotype. The suppression of the aberrant organ positions in knat6 pny double mutant is likely attributable to the misexpression of KNAT6 in pny pedicels as the downregulation of KNAT6 is maintained in pny inflorescence meristems. Removal of KNAT2 activity has an effect only in the absence of both BP and PNY [93]. Further studies involving other TALE heterodimers have indicated that PNY/PNF, PNF/BP, PNY/STM and PNF/STM heterodimers regulate internode patterning or phyllotaxis [18,94].

6 TALE proteins regulate the transition to flowering

The control of the transition from vegetative to reproductive growth integrates environmental (temperature, day-length) and endogenous signals. The so-called autonomous pathway involves an array of regulators that promote flowering independently of day-length, via the downregulation of the floral repressor FLOWERING LOCUS C (FLC). In addition, the impact of day-length on flowering involves FT, a promoter of flowering under long days, which is repressed by FLC [95–97].

The BELL protein ATH1 has been shown to act as a floral repressor regulating FLOWERING LOCUS C (FLC) expression levels [20]. Antagonistic roles for two other BELL members in flower transition has been suggested, as plants overexpressing BELL-like HOMEODOMAIN 3 (BLH3) are flowering early and plants overexpressing BLH6 are delayed in flowering [31]. Double mutants in which both PNY and PNF activities are compromised do not flower and show reduced levels of LEAFY (LFY), APETALA1 (AP1) and CAULIFLOWER (CAL) transcripts [18,98]. Conversely, AG has been found to be a direct target of PNY [17]. Consistent with this, ectopic expression of LFY restores flower formation in pny pnf double mutant. In contrast, ectopic expression of FT in pny pnf could not activate the floral meristem identity genes and thus promote flower specification suggesting that FT may require the function of PNY and PNF to initiate flower formation [98]. In addition to this function, PNY and PNF function in parallel with LEAFY, UNUSUAL FLORAL ORGAN and WUSCHEL to regulate flower identity [99]. Interestingly, PNY acts as repressor of flowering when interacting with ATH1, whereas it acts as a positive regulator of flowering when interacting with PNF [18,22,98].

To conclude, several BELL members have been shown to control the transition from vegetative to the reproductive phase. How the network operates is not completely elucidated, but the identification of direct targets, like AG for PNY, should help integrate these members in the larger flower transition network.

7 TALE proteins control ovule and fruit development

In contrast to the shoot apical meristem, the flower meristem is a determinate structure (i.e. it produces a limited number of organs) [100]. Meristematic activity ceases after the initiation of the last floral organs, the carpels. Later, carpels differentiate in turn a specialized meristematic tissue, the placenta, which lies along the inner side of the replum and which produces ovules. Consistent with this, STM, BP and PNY are expressed in the replum and it was found that AS1 restricts BP expression to the replum to promote correct valve differentiation, further suggesting the presence of conserved regulatory mechanisms for TALE proteins between the shoot meristem and the carpel [101]. From their mutant phenotype, PNY and BP promote replum identity [15,101]. In contrast, KNAT6 is expressed in the boundaries between the replum and the valves and its inactivation suppresses the replum defect seen in pny and in bp pny [93]. This further illustrates distinct and antagonistic interactions between these members.

The BEL1 gene is expressed in ovule integument primordia and controls integument ovule identity [12]. The bel1 mutant exhibits bell-shaped ovules caused by the absence of a true integument [102,103]. Recently it has been shown that BEL1 interacts with several MADS-box factors to control cell fate in ovule primordia [104]. Interestingly, some of the abnormal integuments in bel1 are converted into carpeloid structures [102,103]. Overexpression of KNAT2 and STM also leads to the homeotic conversion of ovules into carpeloid structures and missexpression of BP/KNAT1 alters outer integument morphology [36,105,106]. As the class I KNOX genes are not expressed in ovules and knowing that BEL1 interacts with STM and KNAT2 in yeast two-hybrid assays, it is likely that when overexpressed they disrupt the interaction between BEL1 and the MADS factors. Similarly, a KNOX-BELL heterodimer has been involved in embryo sac development as well. In the blh1/eostre-1 mutant, two egg cells are formed instead of place of one, and one synergid cell is missing. Two-hybrid studies revealed that KNAT3 forms heterodimers with BLH1 [107,108]. Consistent with this, the inactivation of KNAT3 rescues the embryo sac defects of eostre 1 mutant [108]. The exact role of the BLH1-KNAT3 heterodimer in embryo sac development is, however, indirect since BLH1 is not expressed in the embryo sac.

8 Concluding remarks: further TALES for TALES!

In the past two decades, progress has been made towards elucidating the role of TALE proteins in plant development. These proteins regulate many aspects of plant development and have overlapping, distinct, and in some cases antagonistic activities (Fig. 2).

Fig. 2

TALE proteins involvement throughout the Arabidopsis life cycle: (SAM: Shoot apical meristem; IM: Inflorescence meristem; FM: Floral meristem). This figure summarizes the different functions of 9 TALE proteins (out of 21) at each step of Arabidopsis life. For further detail, see text.

However, the functions for half of the TALE members remain unknown. In particular, our knowledge of the KNAT class II members is very limited except for KNAT7 for which a role in secondary wall biosynthesis has been proposed [109,110]. KNAT3, KNAT4 and KNAT5 are expressed in the root but their role remains unclear as loss-of-function mutants and overexpressors for KNAT3, KNAT4 and KNAT5 have wild-type phenotypes [111–113]. Their function may be obscured by redundancy with other factors within the TALE family.

Alternatively, investigation of the functions of the TALE proteins in specific cell types or species could reveal new and/or specific TALE dependent mechanisms. This was recently illustrated in the green alga Chlamydomonas reinhardtii where a KNOX ortholog present in the minus gamete and a BELL ortholog present in the plus gamete heterodimerize in the zygote to activate its developmental program [114]. From an evolutionary perspective, this also shows that, while the TALE proteins are associated with meristem activity in flowering plants, they have other roles in their ancestors. This is also true in multicellular organisms: TALE orthologs have been found to control sporophytic development in the moss Physcomistrella patens, despite the absence of a meristem during this phase [115,116].

While molecular genetics approaches have been successful in unraveling TALE functions, the exact cellular mechanism behind their morphogenetic function remains unclear. The regulation of TALE functions seems to involve an elaborate mechanism that controls TALE protein localization between cells. In particular, microinjection and graft experiments showed that the KN1 protein could move through the plasmodesmata and transport its own mRNA [117]. Furthermore, the microtubule-associated Movement Protein Binding Protein 2C binds to the homeodomain of KN1 and prevents KN1 from moving from cell to cell by restricting its accessibility to plasmodesmata [118]. Last, complementation experiments have shown that KNOX proteins differ in their trafficking ability. Movement was observed for STM and BP, although BP was less motile, but not for KNAT2 and KNAT6 [119,120]. The exact role of this intercellular motility and putative KNOX gradient remain to be elucidated. Inside the cell, OVATE proteins have been shown to interact with KNOX-BELL heterodimers and the cytoskeleton to move the TALE complex from the nucleus to the cytoplasm [107].

The mechanisms and implications behind the spatial control of the TALE proteins in tissues are still far from being completely elucidated. Since these proteins function as heterodimers, it will be essential to determine the exact localization of BELL-KNOX dimers and to identify their specific and overlapping targets to further understand their role. This network becomes even more complex considering that each protein can have distinct protein partners and the resulting heterodimers can exhibit contrasting activities.

More generally, the elucidation of the different layers of regulations and interactions of the TALE proteins has built one of the best documented gene networks in plant development. The flip side is that this network reaches such a level of complexity that it will become increasingly difficult to address its functions, dynamics and interactions using traditional approaches. Prospects for future research should thus involve the integration of the TALE functions in the larger gene regulatory network in virtual tissues using systems biology approaches.


We thank Patrick Laufs and Elisabeth Crowell for a critical reading of the review.


[1] M. Ito; Y. Sato; M. Matsuoka Involvement of homeobox genes in early body plan of monocot, Int. Rev. Cytol., Volume 218 (2002), pp. 1-35

[2] S. Hake; H.M. Smith; H. Holtan; E. Magnani; G. Mele; J. Ramirez The role of KNOX genes in plant development, Ann. Rev. Cell. Dev. Biol., Volume 20 (2004), pp. 125-151

[3] S. Scofield; J.A. Murray KNOX gene function in plant stem cell niches, Plant Mol. Biol., Volume 60 (2006), pp. 929-946

[4] E. Bertolino; B. Reimund; D. Wildt-Perinic; R.G. Clerc A novel homeobox protein which recognizes a TGT core and functionally interferes with a retinoid-responsive motif, J. Biol. Chem., Volume 270 (1995), pp. 31178-31188

[5] T.R. Burglin Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals, Nucl. Acids Res., Volume 25 (1997), pp. 4173-4180

[6] T.R. Burglin The PBC domain contains a MEINOX domain: coevolution of Hox and TALE homeobox genes, Dev. Genes Evol., Volume 208 (1998), pp. 113-116

[7] J. Traas; T. Vernoux The shoot apical meristem: the dynamics of a stable structure, Philos Trans. R. Soc. Lond. B Biol. Sci., Volume 357 (2002), pp. 737-747

[8] M. Aida; M. Tasaka Genetic control of shoot organ boundaries, Curr. Opin. in Plant Biol., Volume 9 (2006), pp. 72-77

[9] M.I. Rast; R. Simon The meristem-to-organ boundary: more than an extremity of anything, Curr. Opin. Genet. Dev., Volume 18 (2008), pp. 287-294

[10] A. Bleckmann; R. Simon Interdomain signaling in stem cell maintenance of plant shoot meristems, Mol. Cells, Volume 27 (2009), pp. 615-620

[11] E. Magnani; S. Hake KNOX Lost the OX: The Arabidopsis KNATM Gene Defines a Novel Class of KNOX Transcriptional Regulators Missing the Homeodomain, Plant Cell, Volume 20 (2008), pp. 875-887

[12] L. Reiser; Z. Modrusan; L. Margossian; A. Samach; N. Ohad; G.W. Haughn; R.L. Fischer The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium, Cell, Volume 83 (1995), pp. 735-742

[13] H.M. Smith; S. Hake The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence, Plant Cell, Volume 15 (2003), pp. 1717-1727

[14] M.E. Byrne; A.T. Groover; J.R. Fontana; R.A. Martienssen Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER, Development, Volume 130 (2003), pp. 3941-3950

[15] A.H. Roeder; C. Ferrandiz; M.F. Yanofsky The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit, Curr. Biol., Volume 13 (2003), pp. 1630-1635

[16] A.M. Bhatt; J.P. Etchells; C. Canales; A. Lagodienko; H. Dickinson VAAMANA--a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis, Gene, Volume 328 (2004), pp. 103-111

[17] X. Bao; R.G. Franks; J.Z. Levin; Z. Liu Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems, Plant Cell, Volume 16 (2004), pp. 1478-1489

[18] H.M. Smith; B.C. Campbell; S. Hake Competence to respond to floral inductive signals requires the homeobox genes PENNYWISE and POUND-FOOLISH, Curr. Biol., Volume 14 (2004), pp. 812-817

[19] R. Kumar; K. Kushalappa; D. Godt; M.S. Pidkowich; S. Pastorelli; S.R. Hepworth; G.W. Haughn The Arabidopsis BEL1-LIKE HOMEODOMAIN Proteins SAW1 and SAW2 Act Redundantly to Regulate KNOX Expression Spatially in Leaf Margins, Plant Cell (2007)

[20] M. Proveniers; B. Rutjens; M. Brand; S. Smeekens The Arabidopsis TALE homeobox gene ATH1 controls floral competency through positive regulation of FLC, Plant J., Volume 52 (2007), pp. 899-913

[21] C. Gomez-Mena; R. Sablowski ARABIDOPSIS THALIANA HOMEOBOX GENE1 establishes the basal boundaries of shoot organs and controls stem growth, Plant Cell, Volume 20 (2008), pp. 2059-2072

[22] B. Rutjens; D. Bao; E. van Eck-Stouten; M. Brand; S. Smeekens; M. Proveniers Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins, Plant J., Volume 58 (2009), pp. 641-654

[23] S.E. Clark; S.E. Jacobsen; J.Z. Levin; E.M. Meyerowitz The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis, Development, Volume 122 (1996), pp. 1567-1575

[24] K. Endrizzi; B. Moussian; A. Haecker; J.Z. Levin; T. Laux The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE, Plant J., Volume 10 (1996), pp. 967-979

[25] J.A. Long; E.I. Moan; J.I. Medford; M.K. Barton A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis, Nature, Volume 379 (1996), pp. 66-69

[26] E. Vollbrecht; B. Veit; N. Sinha; S. Hake The developmental gene Knotted-1 is a member of a maize homeobox gene family, Nature, Volume 350 (1991), pp. 241-243

[27] R.A. Kerstetter; D. Laudencia-Chingcuanco; L.G. Smith; S. Hake Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance, Development, Volume 124 (1997), pp. 3045-3054

[28] E. Vollbrecht; L. Reiser; S. Hake Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1, Development, Volume 127 (2000), pp. 3161-3172

[29] M.E. Byrne; J. Simorowski; R.A. Martienssen ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis, Development, Volume 129 (2002), pp. 1957-1965

[30] E. Belles-Boix; O. Hamant; S.M. Witiak; H. Morin; J. Traas; V. Pautot KNAT6: An Arabidopsis Homeobox Gene Involved in Meristem Activity and Organ Separation, Plant Cell, Volume 18 (2006), pp. 1900-1907

[31] M. Cole; C. Nolte; W. Werr Nuclear import of the transcription factor SHOOT MERISTEMLESS depends on heterodimerization with BLH proteins expressed in discrete subdomains of the shoot apical meristem of Arabidopsis thaliana, Nucl. Acids Res., Volume 34 (2006), pp. 1281-1292

[32] W.H. Chiu; J. Chandler; G. Cnops; M. Van Lijsebettens; W. Werr Mutations in the TORNADO2 gene affect cellular decisions in the peripheral zone of the shoot apical meristem of Arabidopsis thaliana, Plant Mol. Biol., Volume 63 (2007), pp. 731-744

[33] G. Cnops; P. Neyt; J. Raes; M. Petrarulo; H. Nelissen; N. Malenica; C. Luschnig; O. Tietz; F. Ditengou; K. Palme; A. Azmi; E. Prinsen; M. Van Lijsebettens The TORNADO1 and TORNADO2 genes function in several patterning processes during early leaf development in Arabidopsis thaliana, Plant Cell, Volume 18 (2006), pp. 852-866

[34] M. Aida; T. Ishida; M. Tasaka Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes, Development, Volume 126 (1999), pp. 1563-1570

[35] G. Chuck; C. Lincoln; S. Hake KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis, Plant Cell, Volume 8 (1996), pp. 1277-1289

[36] V. Pautot; J. Dockx; O. Hamant; J. Kronenberger; O. Grandjean; D. Jublot; J. Traas KNAT2: evidence for a link between knotted-like genes and carpel development, Plant Cell, Volume 13 (2001), pp. 1719-1734

[37] E. Shani; O. Yanai; N. Ori The role of hormones in shoot apical meristem function, Curr. Opin. Plant. Biol., Volume 9 (2006), pp. 484-489

[38] C. Miller, Skoog, F., von Saltza, MH, Strong, FM. Kinetin. A cell division factor from deoxyribonucleic acid. J. Am. Chem. Soc 77 (1955) 1392–1393.

[39] D.W. Mok; M.C. Mok Cytokinin metabolism and action, Annu. Rev. Plant Physiol. Plant Mol. Biol., Volume 52 (2001), pp. 89-118

[40] J.P. To; J.J. Kieber Cytokinin signaling: two-components and more, Trends Plant Sci., Volume 13 (2008), pp. 85-92

[41] D. Alabadi; M.A. Blazquez; J. Carbonell; C. Ferrandiz; M.A. Perez-Amador Instructive roles for hormones in plant development, Int. J. Dev. Biol. (2008)

[42] H.M. Rupp; M. Frank; T. Werner; M. Strnad; T. Schmulling Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem, Plant J., Volume 18 (1999), pp. 557-563

[43] S. Jasinski; P. Piazza; J. Craft; A. Hay; L. Woolley; I. Rieu; A. Phillips; P. Hedden; M. Tsiantis KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities, Curr. Biol., Volume 15 (2005), pp. 1560-1565

[44] O. Yanai; E. Shani; K. Dolezal; P. Tarkowski; R. Sablowski; G. Sandberg; A. Samach; N. Ori Arabidopsis KNOXI proteins activate cytokinin biosynthesis, Curr. Biol, Volume 15 (2005), pp. 1566-1571

[45] A. Chiappetta; V. Michelotti; M. Fambrini; L. Bruno; M. Salvini; M. Petrarulo; A. Azmi; H. Van Onckelen; C. Pugliesi; M.B. Bitonti Zeatin accumulation and misexpression of a class I knox gene are intimately linked in the epiphyllous response of the interspecific hybrid EMB-2 (Helianthus annuus × H. tuberosus), Planta, Volume 223 (2006), pp. 917-931

[46] T. Sakamoto; N. Kamiya; M. Ueguchi-Tanaka; S. Iwahori; M. Matsuoka KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem, Genes Dev., Volume 15 (2001), pp. 581-590

[47] A. Hay; H. Kaur; A. Phillips; P. Hedden; S. Hake; M. Tsiantis The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans, Curr. Biol., Volume 12 (2002), pp. 1557-1565

[48] H. Chen; A.K. Banerjee; D.J. Hannapel The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1, Plant J., Volume 38 (2004), pp. 276-284

[49] A. Leibfried; J.P. To; W. Busch; S. Stehling; A. Kehle; M. Demar; J.J. Kieber; J.U. Lohmann WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators, Nature, Volume 438 (2005), pp. 1172-1175

[50] S.P. Gordon; V.S. Chickarmane; C. Ohno; E.M. Meyerowitz Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem, Proc. Natl. Acad. Sci. U S A, Volume 106 (2009), pp. 16529-16534

[51] D. Jackson; S. Hake Control of phyllotaxy in maize by the abphyl1 gene, Development, Volume 126 (1999), pp. 315-323

[52] A. Giulini; J. Wang; D. Jackson Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1, Nature, Volume 430 (2004), pp. 1031-1034

[53] B.H. Lee; R. Johnston; Y. Yang; A. Gallavotti; M. Kojima; B.A. Travencolo; F. Costa Lda; H. Sakakibara; D. Jackson Studies of aberrant phyllotaxy1 mutants of maize indicate complex interactions between auxin and cytokinin signaling in the shoot apical meristem, Plant Physiol., Volume 150 (2009), pp. 205-216

[54] D. Weiss; N. Ori Mechanisms of cross talk between gibberellin and other hormones, Plant Physiol., Volume 144 (2007), pp. 1240-1246

[55] M.J. Scanlon The polar auxin transport inhibitor N-1-naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize, Plant Physiol., Volume 133 (2003), pp. 597-605

[56] M. Furutani; T. Vernoux; J. Traas; T. Kato; M. Tasaka; M. Aida PINFORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis, Development, Volume 131 (2004), pp. 5021-5030

[57] A. Hay; M. Barkoulas; M. Tsiantis ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis, Development, Volume 133 (2006), pp. 3955-3961

[58] M.G. Heisler; C. Ohno; P. Das; P. Sieber; G.V. Reddy; J.A. Long; E.M. Meyerowitz Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis Inflorescence eristem, Curr. Biol., Volume 15 (2005), pp. 1899-1911

[59] P.B. de Reuille; I. Bohn-Courseau; K. Ljung; H. Morin; N. Carraro; C. Godin; J. Traas Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis, Proc. Natl. Acad. Sci. U S A, Volume 103 (2006), pp. 1627-1632

[60] L. Borghi; M. Bureau; R. Simon Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity, Plant Cell, Volume 19 (2007), pp. 1795-1808

[61] O. Hamant; F. Nogue; E. Belles-Boix; D. Jublot; O. Grandjean; J. Traas; V. Pautot The KNAT2 homeodomain protein interacts with ethylene and cytokinin signaling, Plant Physiol, Volume 130 (2002), pp. 657-665

[62] D. Hareven; T. Gutfinger; A. Parnis; Y. Eshed; E. Lifschitz The making of a compound leaf: genetic manipulation of leaf architecture in tomato, Cell, Volume 84 (1996), pp. 735-744

[63] M.E. Byrne; R. Barley; M. Curtis; J.M. Arroyo; M. Dunham; A. Hudson; R.A. Martienssen Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis, Nature, Volume 408 (2000), pp. 967-971

[64] E. Semiarti; Y. Ueno; H. Tsukaya; H. Iwakawa; C. Machida; Y. Machida The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves, Development, Volume 128 (2001), pp. 1771-1783

[65] H. Li; L. Xu; H. Wang; Z. Yuan; X. Cao; Z. Yang; D. Zhang; Y. Xu; H. Huang The Putative RNA-Dependent RNA Polymerase RDR6 Acts Synergistically with ASYMMETRIC LEAVES1 and 2 to Repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis Leaf Development, Plant Cell, Volume 17 (2005), pp. 2157-2171

[66] N. Ori; Y. Eshed; G. Chuck; J.L. Bowman; S. Hake Mechanisms that control knox gene expression in the Arabidopsis shoot, Development, Volume 127 (2000), pp. 5523-5532

[67] S.P. Grigg; C. Canales; A. Hay; M. Tsiantis SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis, Nature, Volume 437 (2005), pp. 1022-1026

[68] L. Yang; W. Huang; H. Wang; R. Cai; Y. Xu; H. Huang Characterizations of a Hypomorphic Argonaute1 Mutant reveal novel AGO1 functions in Arabidopsis Lateral Organ Development, Plant Mol. Biol., Volume 61 (2006), pp. 63-78

[69] M.K. Kumaran; J.L. Bowman; V. Sundaresan YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis, Plant Cell, Volume 14 (2002), pp. 2761-2770

[70] C.M. Ha; G.T. Kim; B.C. Kim; J.H. Jun; M.S. Soh; Y. Ueno; Y. Machida; H. Tsukaya; H.G. Nam The BLADE ON PETIOLE1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis, Development, Volume 130 (2003), pp. 161-172

[71] M. Norberg; M. Holmlund; O. Nilsson The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs, Development, Volume 132 (2005), pp. 2203-2213

[72] C.M. Ha; J.H. Jun; H.G. Nam; J.C. Fletcher BLADE ON PETIOLE1 and 2 Control Arabidopsis Lateral Organ Fate through regulation of LOB domain and adaxial-abaxial polarity genes, Plant Cell, Volume 19 (2007), pp. 1809-1825

[73] M. Guo; J. Thomas; G. Collins; M.C. Timmermans Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis, Plant Cell, Volume 20 (2008), pp. 48-58

[74] A. Katz; M. Oliva; A. Mosquna; O. Hakim; N. Ohad FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development, Plant J., Volume 37 (2004), pp. 707-719

[75] D. Schubert; L. Primavesi; A. Bishopp; G. Roberts; J. Doonan; T. Jenuwein; J. Goodrich Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27, EMBO J., Volume 25 (2006), pp. 4638-4649

[76] L. Xu; W.H. Shen Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis, Curr. Biol., Volume 18 (2008), pp. 1966-1971

[77] N. Uchida; S. Kimura; D. Koenig; N. Sinha Coordination of leaf development via regulation of KNOX1 genes, J. Plant Res. (2009)

[78] T. Blein; A. Hasson; P. Laufs Leaf development: what it needs to be complex, Curr. Opin. Plant Biol. (2009)

[79] G. Bharathan; T.E. Goliber; C. Moore; S. Kessler; T. Pham; N.R. Sinha Homologies in leaf form inferred from KNOXI gene expression during development, Science, Volume 296 (2002), pp. 1858-1860

[80] A. Hay; M. Tsiantis The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta, Nat. Genet., Volume 38 (2006), pp. 942-947

[81] M. Barkoulas; A. Hay; E. Kougioumoutzi; M. Tsiantis A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta, Nat. Genet., Volume 40 (2008), pp. 1136-1141

[82] N. Uchida; B. Townsley; K.H. Chung; N. Sinha Regulation of SHOOT MERISTEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development, Proc. Natl. Acad. Sci. U S A, Volume 104 (2007), pp. 15953-15958

[83] S. Kimura; D. Koenig; J. Kang; F.Y. Yoong; N. Sinha Natural variation in leaf morphology results from mutation of a novel KNOX gene, Curr. Biol., Volume 18 (2008), pp. 672-677

[84] H. Jonsson; M.G. Heisler; B.E. Shapiro; E.M. Meyerowitz; E. Mjolsness An auxin-driven polarized transport model for phyllotaxis, Proc. Natl. Acad. Sci. U S A, Volume 103 (2006), pp. 1633-1638

[85] S. Stoma; M. Lucas; J. Chopard; M. Schaedel; J. Traas; C. Godin Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development, PLoS Comput. Biol., Volume 4 (2008), p. e1000207

[86] R.S. Smith; E.M. Bayer Auxin transport-feedback models of patterning in plants, Plant Cell Environ., Volume 32 (2009), pp. 1258-1271

[87] D. Jackson; B. Veit; S. Hake Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot, Development, Volume 120 (1994), pp. 405-413

[88] A. Peaucelle; H. Morin; J. Traas; P. Laufs Plants expressing a miR164-resistant CUC2 gene reveal the importance of post-meristematic maintenance of phyllotaxy in Arabidopsis, Development, Volume 134 (2007), pp. 1045-1050

[89] P. Sieber; F. Wellmer; J. Gheyselinck; J.L. Riechmann; E.M. Meyerowitz Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness, Development, Volume 134 (2007), pp. 1051-1060

[90] S.J. Douglas; G. Chuck; R.E. Dengler; L. Pelecanda; C.D. Riggs KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis, Plant Cell, Volume 14 (2002), pp. 547-558

[91] S.P. Venglat; T. Dumonceaux; K. Rozwadowski; L. Parnell; V. Babic; W. Keller; R. Martienssen; G. Selvaraj; R. Datla The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis, Proc. Natl. Acad. Sci. U S A, Volume 99 (2002), pp. 4730-4735

[92] G. Mele; N. Ori; Y. Sato; S. Hake The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways, Genes Dev., Volume 17 (2003), pp. 2088-2093

[93] L. Ragni; E. Belles-Boix; M. Gunl; V. Pautot Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis Inflorescences, Plant Cell, Volume 20 (2008), pp. 888-900

[94] S. Kanrar; O. Onguka; H.M. Smith Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers, Planta, Volume 224 (2006), pp. 1163-1173

[95] G.G. Simpson The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time, Curr. Opin. Plant. Biol., Volume 7 (2004), pp. 570-574

[96] F. Turck; F. Fornara; G. Coupland Regulation and identity of florigen: FLOWERING LOCUS T moves center stage, Ann. Rev. Plant Biol., Volume 59 (2008), pp. 573-594

[97] C.M. Alexandre; L. Hennig FLC or not FLC: the other side of vernalization, J. Exp. Bot., Volume 59 (2008), pp. 1127-1135

[98] S. Kanrar; M. Bhattacharya; B. Arthur; J. Courtier; H.M.S. Smith Regulatory networks that function to specify flower meristems require the function of homeobox genes PENNYWISE and POUND-FOOLISH in Arabidopsis, The Plant J., Volume 54 (2008), pp. 924-937

[99] L. Yu; V. Patibanda; H.M. Smith A novel role of BELL1-like homeobox genes, PENNYWISE and POUND-FOOLISH, in floral patterning, Planta, Volume 229 (2009), pp. 693-707

[100] R. Sablowski Flowering and determinacy in Arabidopsis, J. Exp. Bot., Volume 58 (2007), pp. 899-907

[101] H. Alonso-Cantabrana; J.J. Ripoll; I. Ochando; A. Vera; C. Ferrandiz; A. Martinez-Laborda Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene, Development, Volume 134 (2007), pp. 2663-2671

[102] K. Robinson-Beers; R.E. Pruitt; C.S. Gasser Ovule Development in Wild-Type Arabidopsis and Two Female-Sterile Mutants, Plant Cell, Volume 4 (1992), pp. 1237-1249

[103] Z. Modrusan; L. Reiser; K.A. Feldmann; R.L. Fischer; G.W. Haughn Homeotic transformation of ovules into Carpel-like structures in Arabidopsis, Plant Cell, Volume 6 (1994), pp. 333-349

[104] V. Brambilla; R. Battaglia; M. Colombo; S. Masiero; S. Bencivenga; M.M. Kater; L. Colombo Genetic and molecular interactions between BELL1 and MADS-box factors support ovule development in Arabidopsis, Plant Cell, Volume 19 (2007), pp. 2544-2556

[105] S. Scofield; W. Dewitte; J.A.H. Murray The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis, The Plant J, Volume 50 (2007), pp. 767-781

[106] E. Truernit; J. Haseloff Arabidopsis thaliana outer ovule integument morphogenesis: Ectopic expression of KNAT1 reveals a compensation mechanism, BMC Plant Biol., Volume 8 (2008), p. 35

[107] J. Hackbusch; K. Richter; J. Muller; F. Salamini; J.F. Uhrig A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins, Proc. Natl. Acad. Sci. U S A, Volume 102 (2005), pp. 4908-4912

[108] G.C. Pagnussat; H.J. Yu; V. Sundaresan Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1, Plant Cell, Volume 19 (2007), pp. 3578-3592

[109] D.M. Brown; L.A. Zeef; J. Ellis; R. Goodacre; S.R. Turner Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics, Plant Cell, Volume 17 (2005), pp. 2281-2295

[110] R. Zhong; C. Lee; J. Zhou; R.L. McCarthy; Z.H. Ye A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis, Plant Cell, Volume 20 (2008), pp. 2763-2782

[111] K. Serikawa; A. Martinez-Laborda; P.C. Zambryski Three knottedl-like homeobox genes in Arabidopsis Plant Mol, Biol., Volume 32 (1996), pp. 673-683

[112] K. Serikawa; A. Martinez-Laborda; H. Kim Localization of expression of KNAT3, a class 2 knotted1-like gene, The Plant J., Volume 11 (1997), pp. 853-861

[113] E. Truernit; K.R. Siemering; S. Hodge; V. Grbic; J. Haseloff A map of KNAT gene expression in the Arabidopsis root, Plant Mol. Biol, Volume 60 (2006), pp. 1-20

[114] J.H. Lee; H. Lin; S. Joo; U. Goodenough Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family, Cell, Volume 133 (2008), pp. 829-840

[115] S.D. Singer; N.W. Ashton Revelation of ancestral roles of KNOX genes by a functional analysis of Physcomitrella homologues, Plant Cell Rep., Volume 26 (2007), pp. 2039-2054

[116] K. Sakakibara; T. Nishiyama; H. Deguchi; M. Hasebe Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development, Evol. Dev., Volume 10 (2008), pp. 555-566

[117] W.J. Lucas; S. Bouche-Pillon; D.P. Jackson; L. Nguyen; L. Baker; B. Ding; S. Hake Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata, Science, Volume 270 (1995), pp. 1980-1983

[118] N. Winter; G. Kollwig; S. Zhang; F. Kragler MPB2C, a microtubule-associated protein, regulates non-cell-autonomy of the homeodomain protein KNOTTED1, Plant Cell, Volume 19 (2007), pp. 3001-3018

[119] J.Y. Kim; Z. Yuan; M. Cilia; Z. Khalfan-Jagani; D. Jackson Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis, Proc. Natl. Acad. Sci. U S A, Volume 99 (2002), pp. 4103-4108

[120] J.Y. Kim; Y. Rim; J. Wang; D. Jackson A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking, Genes Dev., Volume 19 (2005), pp. 788-793

[121] M. Bellaoui; M.S. Pidkowich; A. Samach; K. Kushalappa; S.E. Kohalmi; Z. Modrusan; W.L. Crosby; G.W. Haughn The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals, Plant Cell, Volume 13 (2001), pp. 2455-2470

[122] J. Müller; Y. Wang; R. Franzen; L. Santi; F. Salamini; W. Rohde In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function, Plant J., Volume 27 (2001), pp. 13-23

[123] H.M. Smith; I. Boschke; S. Hake Selective interaction of plant homeodomain proteins mediates high DNA binding affinity, Proc. Natl. Acad. Sci. U S A, Volume 99 (2002), pp. 9579-9584

[124] J.A. Long; M.K. Barton The development of apical embryonic pattern in Arabidopsis, Development, Volume 125 (1998), pp. 3027-3035

[125] C. Lincoln; J. Long; J. Yamaguchi; K. Serikawa; S. Hake A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants, Plant Cell, Volume 6 (1994), pp. 1859-1876

[126] S.J. Douglas; C.D. Riggs Pedicel development in Arabidopsis thaliana: contribution of vascular positioning and the role of the BREVIPEDICELLUS and ERECTA genes, Dev. Biol., Volume 284 (2005), pp. 451-463

[127] J. Dockx; N. Quaedvlieg; G. Keultjes; P. Kock; P. Weisbeek; S. Smeekens The homeobox gene ATK1 of Arabidopsis thaliana is expressed in the shoot apex of the seedling and in flowers and inflorescence stems of mature plants, Plant Mol. Biol., Volume 28 (1995), pp. 723-737

[128] G. Dean; S. Casson; K. Lindsey KNAT6 gene of Arabidopsis is expressed in roots and is required for correct lateral root formation, Plant Mol. Biol., Volume 54 (2004), pp. 71-84

[129] N. Quaedvlieg; J. Dockx; F. Rook; P. Weisbeek; S. Smeekens The homeobox gene ATH1 of Arabidopsis is derepressed in the photomorphogenic mutants cop1 and det1, Plant Cell, Volume 7 (1995), pp. 117-129

[130] C. Silva; S. Pelaz Role of atBHL6 in flowering time and floral organ development, 18th ICAR, Beijing, 2007

Comments - Policy