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New insights into the regulation of inflorescence architecture Zhi Wei Norman Teo, Shiyong Song, Yong-Qiang Wang, Jie Liu, and Hao Yu Department of Biological Sciences and Temasek Life Sciences Laboratory, National University of Singapore, 117543 Singapore
The architecture of inflorescences displays the spatiotemporal arrangement of flowers and determines plant reproductive success through affecting fruit set and plant interaction with biotic or abiotic factors. Flowering plants have evolved a remarkable diversity of inflorescence branching patterns, which is largely governed by developmental decisions in inflorescence meristems and their derived meristems between maintenance of indeterminacy and commitment to the floral fate. Recent findings suggest that regulation of inflorescence architecture is mediated by flowering time genes, Arabidopsis LSH1 and Oryza G1 (ALOG) family genes, and the interaction between the auxin pathway and floral meristem regulators. In this review, we discuss how the relevant new players and mechanisms account for the development of appropriate inflorescence structures in flowering plants in response to environmental and developmental signals. Diverse inflorescence architectures in flowering plants During post-embryonic development of flowering plants, the shoot apical meristem (SAM) and root apical meristem (RAM) generate aerial and underground parts, respectively. The SAM gives rise to all aerial organs under a dynamic balance of growth and differentiation. It generates vegetative structures, such as leaves, stems, and axillary meristems, at the vegetative phase and is transformed into the main inflorescence meristem during the floral transition, when environmental and developmental conditions are optimal for plant reproductive success. The main inflorescence meristem either produces flowers or remains indeterminate to produce branch meristems, which could iterate the pattern of the main inflorescence meristem. Various branching patterns and the spatiotemporal generation of flowers from main and branch meristems contribute to a huge variety of inflorescence architectures observed in nature. The optimal inflorescence architecture plays a key part in reproductive success because it affects the ultimate number of flowers that set fruits and the competitive strength of plant individuals in interacting with biotic or abiotic factors, such as pollinators and wind [1–3].
Corresponding author: Yu, H. ([email protected]). 1360-1385/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2013.11.001
There are three major architectural types of inflorescences based on the termination events on the inflorescence meristems of various orders [4,5]. Plants such as Arabidopsis (Arabidopsis thaliana) develop the racemetype inflorescences, in which main inflorescence meristems grow indefinitely and generate either flowers or branch meristems that reiterate the pattern of the main inflorescence meristems (Figure 1). The panicle-type inflorescences are largely characteristic of grasses such as rice (Oryza sativa) and oat (Avena sativa). Main inflorescence meristems of these plants terminate after producing a series of lateral branch meristems, which eventually terminate in flowers after generating either flowers or higher-order branches (Figure 1). Unlike the racemeand panicle-type inflorescences, a cyme-type inflorescence, such as the one that develops in tomato (Solanum lycopersicum), lacks a main axis and terminates in a flower after generating a new inflorescence meristem that reiterates this pattern (Figure 1). In addition to the three architectural types and their variations, two basic growth habits, monopodial and sympodial, affect the diversity in inflorescence architecture. During the floral transition, the main SAMs of monopodial plants, such as Arabidopsis and rice, develop into the central leader inflorescence shoots while producing other subordinate branches. By contrast, the SAMs of sympodial plants, such as tomato, either terminate in reproductive structures or are aborted after a period of vegetative growth, and their growth continues from new axillary meristems that repeat this process. In tomato, the SAM terminates in a cyme-type inflorescence, and new vegetative growth continues from a sympodial shoot meristem produced from the axil of the youngest leaf [6–8]. The sympodial shoot meristem reiterates the pattern of the SAM to terminate in an inflorescence and initiate the generation of a new sympodial shoot meristem, eventually resulting in elaborate sympodial inflorescence shoots in tomato (Figure 1). Recent findings from different plant species have demonstrated that the integrated regulatory network that controls inflorescence architecture includes previously unrecognized components, such as flowering time genes and Arabidopsis LSH1 and Oryza G1 (ALOG) family genes, and an interaction between the auxin pathway and floral meristem regulators. In this review, we discuss how these new components contribute to the development of appropriate inflorescence architectures in flowering plants to ensure reproductive success under changing growth conditions. Trends in Plant Science xx (2013) 1–8
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Figure 1. Comparison of the inflorescence architecture of Arabidopsis, rice and tomato. (A) Schematic diagrams depicting the inflorescence structures of Arabidopsis, rice, and tomato. Brown circles, green arrows, and a green circle represent flowers, indeterminate shoots, and a determinate shoot, respectively. Black arrows indicate canonical axillary shoot meristems in tomato. (B) Sequential development of shoot meristems contributes to different inflorescence structures in Arabidopsis, rice, and tomato. In monopodial plants such as Arabidopsis and rice, during the floral transition the vegetative shoot meristem (VSM) is transformed into the main inflorescence meristem (IM) that subsequently generates all of the other branches and flowers. Arabidopsis develops the raceme-type inflorescence, in which a main IM grows indefinitely and generates either floral meristems (FMs) or primary branch meristems (pBMs) that reiterate the pattern of the main IM to produce either secondary branch meristems (sBMs) or FMs. In the panicle-type inflorescence of rice, the main IM terminates after the production of several pBMs that generate sBMs or spikelet meristems (SMs), each of which is transformed into a single FM. sBMs usually reiterate the pattern of pBMs to give rise to SMs and FMs. Tomato is a typical sympodial plant, in which the VSM terminates in a sympodial IM (SIM), whereas new vegetative growth continues from a sympodial shoot meristem (SYM) produced from the axil of the youngest leaf. The SYM reiterates the pattern of VSM to terminate in a SIM and initiate the generation of a new SYM. The SIM generates a new SIM before terminating in a FM, and reiteration of this pattern forms the cyme-type inflorescence in tomato.
Regulation of meristem identity determines inflorescence architecture Although a remarkable diversity of inflorescence architectures has evolved in flowering plants (Figure 1), the inflorescence branching pattern is mainly dependent on developmental decisions that take place in inflorescence meristems and their derived meristems; within each meristem, a decision is made between the maintenance of indeterminacy and commitment to the floral fate. Previous studies in Arabidopsis have suggested that an antagonistic interaction between the shoot identity gene TERMINAL FLOWER 1 (TFL1) and floral meristem identity genes, such as LEAFY (LFY) and APETALA1 (AP1), regulates the inflorescence branching pattern [9–11]. TFL1 is specifically expressed in the center of the main 2
inflorescence meristem and lateral branch meristems [10,12], whereas LFY and AP1 are strongly expressed in young floral meristems [13–16]. Loss of function of TFL1 results in early flowering and the conversion of the main inflorescence meristem and lateral branch meristems into floral meristems, which is accompanied with ectopic expression of LFY and AP1 in these meristems [9,17–19]. By contrast, the opposite phenotypes of late flowering and highly branched inflorescences are observable in transgenic plants overexpressing TFL1, in which upregulation of LFY and AP1 during the floral transition is delayed [12]. These results suggest that TFL1 activity is responsible for indeterminate growth of inflorescence meristems partly through preventing the meristems from acquiring the floral identity promoted by LFY and AP1. Conversely, floral meristem identity genes, such as LFY, AP1, and two AP1 homologs, CAULIFLOWER (CAL) and FRUITFULL (FUL), are required to repress TFL1 expression in floral meristems [10,11,19–21]. In the absence of these floral meristem identity genes, ectopic and/or upregulated expression of TFL1 contributes to the conversion of floral meristems into inflorescence shoots. Thus, TFL1 and floral meristem identity genes contribute to shaping the inflorescence architecture in Arabidopsis through antagonizing each other to determine the identity of inflorescence meristems and their derived meristems (Figure 2A). LFY encodes a plant-specific transcription factor, the orthologs of which are present as single-copy genes in most land plant species [22]. Although LFY-like genes share two highly conserved domains, their expression patterns and functions are diverse in various plants [23–27]. For example, unlike its counterpart in Arabidopsis, the rice ortholog of LFY, ABERRANT PANICLE ORGANIZATION 2/RICE FLORICAULA (Table 1), is not expressed in floral meristems and has a role in suppressing the transition from inflorescence meristems to floral meristems [28–30]. It has been proposed that LFY-like genes might have two functions: an ancestral role in promoting meristematic growth and a novel role in mediating floral identity [24]. These two functions might exist with different strengths under different regulatory contexts in most flowering plants, thus contributing to various inflorescence structures observed in nature. Whereas LFY-like genes occur in most land plants, AP1 orthologs belong to the euAP1 gene clade of MADS-box genes and are only present in the core eudicots that comprise the majority of extant angiosperm species [31]. The expression and function of AP1-like genes are usually related to flower development [4], whereas their functional modes differ in various plants. For example, AP1 is required for establishment of floral meristems in Arabidopsis, whereas the counterparts in rice, OsMADS14, OsMADS15, and OsMADS18 (Table 1), are involved in specifying inflorescence meristems rather than floral meristems [32]. TFL1 is a member of the CETS (CENTRORADIALIS, TFL1, and SELF-PRUNING) family proteins that have homology with highly conserved phosphatidylethanolamine-binding proteins (PEBPs) in eukaryotes [33,34]. So far, investigations on TFL1 orthologs in various plant species have shown that these genes have a relatively conserved role in affecting inflorescence architecture through preventing shoot meristems from differentiating
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Figure 2. Modulation of TERMINAL FLOWER1 (TFL1) expression determines inflorescence architecture. (A) Model for the regulatory network that determines inflorescence branching in Arabidopsis. The commitment of lateral branch meristems (BMs) from the inflorescence meristem (IM) to indeterminate shoots or determinate flowers contributes to the inflorescence branching pattern. In Arabidopsis, this developmental transition is determined by antagonistic interactions between the shoot identity regulator TFL1 and a group of regulators involved in mediating the acquisition of floral meristem (FM) identity, including LEAFY (LFY), APETALA1 (AP1), SHORT VEGETATIVE PHASE (SVP), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), AGAMOUS-LIKE 24 (AGL24), and SEPALLATA 4 (SEP4). The flowering time genes, SVP, SOC1, and AGL24, are suppressed by AP1 in emerging FMs, but their expression at appropriate levels in FMs is indispensable for AP1 to suppress TFL1 [38,56– 58]. SEP4 is suppressed by SVP, SOC1, or AGL24, but otherwise has a redundant role in suppressing TFL1 [38]. AP1 interacts with SVP, SOC1, AGL24, or SEP4 in vivo, and all of these MADS-box transcription factors bind to the overlapping 30 region of the TFL1 locus that is also associated with LFY [38,45]. LFY and AP1 promote mutual mRNA expression in FMs, whereas the auxin pathway induces LFY that in turn affects auxin biosynthesis, transport, and signaling [11,25,26,45,77], as illustrated in Figure 3. Arrows and T bars indicate promoting and repressive effects, respectively. The double-ended diamond arrow indicates a feedback regulation between LFY and the auxin pathway. (B) Comparison of the inflorescence architecture between an Arabidopsis wild-type (WT) plant (Columbia) and a tfl1 loss-of-function mutant. (C) Comparison of the inflorescence architecture between a WT (cv. Nipponbare) and a transgenic rice plant in which four rice RICE CENTRORADIALIS (RCN) genes are knocked down through RNA interference (RNAi).
into floral meristems (Figure 2B,C) [35–39]. Of the 19 known PEBPs in rice, four [RICE CENTRORADIALIS 1–4 (RCN1–4)] are closely related to TFL1 [40]. Overexpression of RCNs causes a late flowering and highly branching phenotype [37,41], whereas knocking down RCNs results in much smaller panicles with reduced branches in rice (Figure 2C) [38]. These observations, together with the studies on TFL1-like genes in various plant species [4], suggest that TFL1-like genes may have a general role in maintaining the indeterminacy of shoot meristems. In Arabidopsis, it has been proposed that TFL1 might antagonize another floral pathway integrator, FLOWERING LOCUS T (FT), to act as a transcriptional repressor through interacting with a bZIP transcription factor, FD, and negatively modulating FD-dependent transcription of downstream genes, including those involved in the regulation of floral meristem specification [42]. Many efforts have been made to understand the dynamic subcellular localization of TFL1 during Arabidopsis
development in order to elucidate the mechanisms by which TFL1 regulates downstream genes. Interestingly, experiments performed in several laboratories have obtained different and even opposite results, revealing TFL1 localization in a range of locations, including the cytoplasm, nucleus, and endomembrane compartments [42–44]. Because subcellular localization is essential for developmental regulators, such as TFL1, to exert their function, it is fundamentally important in future studies to address these discrepancies, which could be attributed to different antibodies and/or expression levels of the TFL1 protein in various experimental systems. Flowering time genes are important players in regulating inflorescence architecture Although it remains largely unknown how TFL1-like proteins affect downstream genes, intensive studies in Arabidopsis have provided significant insights into the regulation of TFL1 expression during the floral transition. 3
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Table 1. List of major genes that affect floral meristem identity and inflorescence architecture in Arabidopsis, and their orthologs in rice and tomato Arabidopsis gene TERMINAL FLOWER1 (TFL1)
Protein PEBP family protein
Function Maintains shoot identity
LEAFY (LFY)
Plant-specific TF
Promotes FM identity and floral organ patterning
APETALA1 (AP1)
MADS-box TF
Promotes FM identity and floral organ patterning
SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) AGAMOUS-LIKE 24 (AGL24); SHORT VEGETATIVE PHASE (SVP) SEPALLATA 4 (SEP4)
MADS-box TF
Mediates flowering time, FM specification, and floral organ patterning Mediates flowering time, FM specification, and floral organ patterning
OsMADS50; OsMADS56
Mediates flowering time, and FM and floral organ identity
MADS-box TF
MADS-box TF
Rice ortholog RICE CENTRORADIALIS1–4 (RCN1–4) ABERRANT PANICLE ORGANIZATION 2 (APO2)/RICE FLORICAULA (RFL) OsMADS14; OsMADS15; OsMADS18
Tomato ortholog SELF-PRUNING (SP)
Refs [9–11,17,18]
FALSIFLORA (FA)
[13–15,25,26,77]
MACROCALYX (MC); TM4; SLMBP7 (FUL2); SLMBP20 TM3; SLMBP14; SLMBP18
[16,19,38, 45,50,56]
OsMADS22; OsMADS47; OsMADS55
JOINTLESS; SLMBP24
[38,48,50,56–58]
OsMADS34
TM29; RIPENING INHIBITOR (RIN); TM5; LeMADS1; SLMBP21
[38,55]
[38,49,56,58]
Abbreviations: FM, floral meristem; IM, inflorescence meristem; PEBP, phosphatidylethanolamine-binding protein; SLMBP, SOLANUM LYCOPERSICUM MADS-BOX PROTEIN; TF, transcription factor; TM, TOMATO MADS-BOX.
Molecular genetic evidence suggests that AP1 and LFY are two upstream repressors of TFL1 in floral meristems [10,11,20,21]. Both AP1 and LFY are associated with an overlapping 30 region of the TFL1 gene, implying that they might interact to directly suppress TFL1 expression [45–47]. A recent study has revealed that a set of MADS-box transcription factors, namely SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), SHORT VEGETATIVE PHASE (SVP), AGAMOUS-LIKE 24 (AGL24), and SEPALLATA 4 (SEP4), act redundantly and directly to suppress TFL1 in emerging floral meristems [38] (Figure 2A). In the soc1-2 agl24-3 svp-41 sep4-1 quadruple loss-of-function mutant, the main inflorescence meristem continuously generates secondary and tertiary branch shoots, resulting in a massive inflorescence branching phenotype. Although AP1 and LFY are normally expressed in the anlagen of branch meristems in the mutant, they are unable to suppress the persistent expression of TFL1, which eventually confers shoot identity rather than floral identity on branch meristems. These observations indicate that SVP, SOC1, AGL24, or SEP4 is indispensable for the well-known function of AP1 and LFY in repressing TFL1. Chromatin immunoprecipitation and coimmunoprecipitation assays have shown that SVP, SOC1, AGL24, or SEP4 interacts with AP1 and directly binds to the 30 region of the TFL1 locus that overlaps with the region bound by both AP1 and LFY [38,45–47]. Among these four MADS-box transcription factors, SVP is a dominant regulator that suppresses TFL1 in wild-type inflorescence apices, whereas SOC1 and AGL24 exert similar repressive function in svp-41 mutants [38]. SEP4 is ectopically expressed in the inflorescence meristem of soc1-2 agl24-3 svp-41 mutants and acts as the main regulator for suppressing TFL1 only in the absence of SVP, SOC1, and AGL24. Thus, these MADS-box genes have redundant roles in regulating TFL1 expression in different genetic backgrounds. 4
SVP, SOC1, and AGL24 were first identified as important flowering time genes that regulate the floral transition in Arabidopsis [48–50]. SVP acts as a potent flowering repressor that interacts with another repressor, FLOWERING LOCUS C, to suppress the expression of two floral pathway integrators, FT and SOC1 [48,51,52]. By contrast, both SOC1 and AGL24 respond to multiple flowering genetic signals and interact with each other to promote flowering [49,50,53,54]. SEP4, which was first reported as a class E floral organ identity gene involved in the control of floral meristem and organ identity [55], also has a redundant role with other flowering promoters in regulating flowering (J. Liu et al., unpublished). Therefore, prior to their function in floral meristems, these genes are part of the regulatory network that determines the timing of the transition from vegetative to reproductive growth. In emerging floral meristems, the expression of SVP, SOC1, and AGL24 is downregulated by AP1 to appropriate levels to prevent the reversion of floral meristems into various shoot structures [56,57]. Expression of SVP, SOC1, and AGL24 at appropriate levels seems to have dual roles in this specific developmental context. On the one hand, they act redundantly with SEP4 to interact with AP1 to suppress the expression of the common target TFL1, thus eventually enabling the acquisition of floral identity in branch meristems [38]. On the other hand, SVP, SOC1, and AGL24 also directly repress the expression of SEP3, another class E floral organ identity gene that acts with LFY to activate class B and C gene expression, thus determining the timing of floral organ patterning by preventing premature differentiation of floral meristems into floral organs [58,59]. These results demonstrate a delicate mechanism through which SVP, SOC1, and AGL24 secure the development of a branch anlage into a transiently indeterminate meristem. This transient phase of indeterminacy not only prevents the branch meristem from reverting back to the shoot meristem but also permits the
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Review meristem to subsequently develop into a larger floral meristem containing sufficient cells for proper patterning of whorled organs by class B and C floral homoeotic genes. Taken together, SVP, SOC1, and AGL24 have crucial and persistent roles in mediating several successive developmental programs during the floral transition, including flowering time control, floral meristem specification, and floral organ patterning, all of which contribute to different extents to shaping the inflorescence architecture. Because the expression of SVP, SOC1, and AGL24 is tightly controlled by various environmental and developmental signals [48–52,54], the coordinated regulatory events mediated by these genes allow Arabidopsis plants to fine-tune the timing of flowering and subsequently develop appropriate inflorescence architectures for timely interaction with biotic or abiotic factors, thus ensuring the reproductive success under changing growth conditions. In rice, enhanced panicle branching with an increased number of higher order branches is observed [38] when the rice orthologs of SOC1 (OsMADS50 and OsMADS56) and SVP/AGL24 (OsMADS22, OsMADS47, and OsMADS55) (Table 1) are downregulated in the panicle phytomer2-1 ( pap2-1) mutant, in which a rice ortholog of SEP4, OsMADS34, is knocked out [60]. This phenotype, which is correlated with ectopic expression of RCN4 in these plants, resembles that exhibited by transgenic rice plants overexpressing RCNs [37,41]. These observations suggest that the interaction of flowering time genes with TFL1-like genes could be a conserved mechanism for regulating inflorescence architecture in dicots and monocots. ALOG family proteins mediate inflorescence architecture In addition to flowering time genes, ALOG family proteins, which are conserved in the plant kingdom with a single small domain of unknown function [61,62], have been recently demonstrated to play a part in mediating inflorescence architecture in both rice and tomato [8,63]. TAWAWA1 (TAW1) encodes one of the ten ALOG family proteins in rice and regulates inflorescence architecture through maintaining an indeterminate fate of inflorescence meristems and suppressing the specification of determinate spikelet meristems that later develop into floral meristems (Figure 1B) [63]. Downregulation of TAW1 causes early termination of inflorescence meristems and precocious formation of spikelet meristems, resulting in small inflorescences with a reduced number of primary branches in rice, whereas upregulation of TAW1 displays an increased branching phenotype because of its opposite effect on the regulation of inflorescence and spikelet meristems. Interestingly, the expression of rice orthologs of SVP (OsMADS22, OsMADS47, and OsMADS55) is upregulated by TAW1, whereas overexpression of OsMADS22 and OsMADS55 mimics the inflorescence phenotype caused by upregulation of TAW1, suggesting that TAW1 modulates inflorescence architecture partly through promoting SVP-like genes [63]. In contrast to SVP-like genes, genes involved in spikelet development, such as OsMADS7 (a SEP3 ortholog), OsMADS3, and OsMADS58 (orthologs of AGAMOUS, an Arabidopsis class C floral organ identity gene), are downregulated by TAW1. This repression could
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be similarly mediated by SVP-like genes, as demonstrated in Arabidopsis, in which SVP suppresses the expression of SEP3 and its downstream floral organ identity genes, including AGAMOUS, in floral meristems [58]. TERMINATING FLOWER (TMF) encodes another ALOG family protein and affects inflorescence organization in tomato [8]. Like TAW1 in rice, TMF maintains meristem indeterminacy and suppresses the adoption of floral fate in the meristem. In tmf loss-of-function mutants, the primary SAMs terminate as single flowers without formation of sympodial inflorescence meristems or vegetative shoot meristems. This is partially attributed to precocious activation of the F-box gene ANANTHA (AN), an ortholog of Arabidopsis UNUSUAL FLORAL ORGANS (UFO), and its transcription factor partner FALSIFLORA (FA), an ortholog of Arabidopsis LFY [8]. In addition, tomato orthologs of AP1 and SEP genes are upregulated in tmf. Thus, TMF affects inflorescence architecture in tomato possibly via preventing early expression of those genes that contribute to promoting floral fate. Whether this regulation is also mediated by SVP-like genes is so far unknown. LIGHT-DEPENDENT SHORT HYPOCOTYLS 3 (LSH3) and LSH4, also known as ORGAN BOUNDARY 1 (OBO1) and OBO4, encode two of the 11 ALOG family proteins in Arabidopsis [64,65]. Both LSH3 and LSH4 are expressed at the boundary of the SAM and lateral organs, which is similar to the expression pattern of TMF in tomato [8]. Ablation of the specific cells expressing LSH3 results in loss of the SAM and lateral organs. Constitutive expression of LSH3 and LSH4 generates ectopic meristems and chimeric floral organs in flowers [64,65]; this partially mimics the phenotype exhibited by mutations in UFO, a gene that shares overlapping expression patterns with LSH3 and LSH4, particularly at the boundary of the SAM [66,67]. Thus, the potential interaction between LSHs and UFO, which is analogous to the relationship between TMF and AN in tomato, could also regulate meristem maintenance and organogenesis in Arabidopsis. Knocking out LSH3 and LSH4 does not result in an obvious phenotype [64], and therefore it will be important to investigate other redundant factors, such as their interacting partners or other ALOG family proteins, to elucidate whether ALOG family proteins affect inflorescence architecture in Arabidopsis. In summary, accumulating evidence on the role of ALOG family proteins in maintaining meristem indeterminacy and suppressing floral identity, together with the unique expression pattern of LSH3, LSH4, and TMF in boundary regions of the SAM, indicates that ALOG family proteins might be an important group of regulators that affect inflorescence architecture through mediating the transition between undifferentiated and differentiated cells in the SAM. Auxin mediates floral initiation and inflorescence architecture Another essential question about inflorescence architecture, which is related to the above discussion on the regulation of meristem identity of lateral branches, is how the growth of branch meristems and their fate specification is 5
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YUC1 YUC4 TAR2 Auxin transport
PIN1 PID
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Auxin signaling
ANT AIL6
Iniaon of floral meristem TRENDS in Plant Science
Figure 3. The auxin pathway and LEAFY (LFY) interact to mediate the initiation of floral primordia. The auxin maximum at floral anlagen is required for the initiation of floral primordia and generated by polar auxin transport involving auxin efflux regulators, such as PIN-FORMED 1 (PIN1) and PINOID (PID) [68,69,71]. In incipient primordia, auxin induces LFY expression through triggering the degradation of INDOLE-3-ACETIC ACID 12/BODENLOS (IAA12/BDL), which physically interacts with and inhibits the activity of MONOPTEROS/AUXIN RESPONSE FACTOR 5 (MP/ ARF5), a protein that directly upregulates LFY and other two transcription factors, AINTEGUMENTA (ANT) and AINTEGUMENTA-LIKE6 (AIL6) [26]. LFY is involved in feedback regulation of the auxin pathway through negatively regulating the expression of several genes involved in auxin biosynthesis [such as YUCCA 1 (YUC1), YUC4, and TAR2] and promoting the expression of the auxin transport regulator PID and auxin signaling [25,26,46,47]. Promoting and repressive effects are indicated by arrows and T bars, respectively. Genes enclosed in colored boxes are transcription factors.
coordinated. Initiation of branch meristems with floral identity on the flanks of the inflorescence meristem is dependent on the auxin maximum at branch anlagen [68,69]. Loss-of-function mutations in the genes involved in auxin biosynthesis, the efflux carrier PIN-FORMED 1 (PIN1), and an AUXIN-RESPONSE FACTOR (ARF) gene MONOPTEROS (MP, also known as ARF5) all abolish floral meristem formation, resulting in naked inflorescence stems in Arabidopsis [70–72]. These observations indicate that auxin biosynthesis, transport, and signaling have an indispensable role in floral meristem initiation and inflorescence organization. Recent evidence has suggested that the interaction between LFY and the auxin pathway coordinates the outgrowth of primordia from the inflorescence meristem and the specification of their floral identity (Figure 3) [25,26]. Auxin activates MP by triggering the degradation of an AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) transcriptional repressor called IAA12/BODENLOS (BDL) that physically interacts with MP and suppresses its activity [26]. In incipient floral primordia, auxin-activated MP directly induces the expression of LFY and two AP2-like transcription factors, AINTEGUMENTA (ANT) and AINTEGUMENTA-LIKE6/PLETHORA3 (AIL6/PLT3) [26]. LFY has a pivotal role in specifying floral meristem identity [13,14], whereas ANT and AIL6 are essential for the growth of floral primordia [73–76]. Thus, auxin-activated MP coordinates fate specification and meristem growth during the initiation of floral primordia. It is noteworthy that LFY is also involved in feedback regulation of the auxin pathway through modulating expression of genes involved in auxin biosynthesis, transport 6
and signaling (Figure 3) [25,26,46,47]. LFY is physically associated with many genes in the auxin pathway [46,47], implying that LFY could directly control the transcription of these genes. Expression analyses have revealed that LFY downregulates several genes involved in auxin biosynthesis, such as YUCCA 1 (YUC1), YUC4, and TRYPTOPHAN AMINOTRANSFERASE RELATED 2 (TAR2) [25], but upregulates the auxin transport regulator PINOID (PID) [26]. In agreement with these expression data, auxin levels are reversely correlated with LFY activity in inflorescence apices [25], whereas LFY promotes auxin accumulation in floral primordia [26]. Furthermore, LFY affects the expression of AUX/IAA genes, such as IAA1, IAA17, and IAA29, and upregulates the expression of the auxin-response reporter DR5rev::3XVenus-N7 or DR5rev::GFP in floral meristems [25,26], indicating that LFY also positively regulates auxin signaling. Positive and negative feedback regulation of auxin biosynthesis, transport and signaling by LFY provides pivotal mechanisms for coordinate and subtle regulation of several successive developmental programs required for the establishment of floral meristems and the resulting inflorescences. Although the heterogeneous distribution of auxin at floral anlagen is important for initiation and growth of primordia, timely induction of LFY by auxin in the primordia not only determines the specification of floral meristem identity but also modulates the auxin level and distribution in developing floral meristems, which is required for subsequent initiation and patterning of various floral organs. Therefore, the interaction between LFY and the auxin pathway integrates auxin signaling into the regulatory network that determines inflorescence branching in Arabidopsis (Figure 2A). Concluding remarks Sustained efforts of many laboratories over the past few years have provided significant insights into the regulation of inflorescence architecture that determines plant reproductive success. Newly recognized components of this regulatory event in various plants species include a set of flowering time genes that have essential roles in coordinating flowering time and subsequent floral meristem development, and ALOG family genes that regulate the meristem identity in the shoot apex. Furthermore, interaction and feedback regulation between the auxin pathway and LFY mediate the initiation and specification of floral meristems, forming an integral part of the regulatory hierarchies required for shaping inflorescence architecture in Arabidopsis. These advances, however, raise further questions that need to be addressed. For example, the interaction between ALOG family proteins and other known floral meristem regulators is still largely unknown. Also, it would be interesting to investigate whether the auxin pathway interacts with other conserved regulators in floral meristems because the functions of LFY orthologs are diverse in flowering plants. We can expect to observe more intertwined feedback loops and new players in the regulation of inflorescence architecture through addressing these questions. Acknowledgments The preparation of this review was supported by the Academic Research Fund (MOE2011-T2-2-008) from the Ministry of Education, Singapore,
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Review the Singapore National Research Foundation under its Competitive Research Programme (NRF2010NRF-CRP002-018), and the intramural resource support from National University of Singapore and Temasek Life Sciences Laboratory. We apologize to those authors whose excellent work could not be cited owing to space limitations.
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Review
New insights into the regulation of inflorescence architecture Zhi Wei Norman Teo, Shiyong Song, Yong-Qiang Wang, Jie Liu, and Hao Yu Department of Biological Sciences and Temasek Life Sciences Laboratory, National University of Singapore, 117543 Singapore
The architecture of inflorescences displays the spatiotemporal arrangement of flowers and determines plant reproductive success through affecting fruit set and plant interaction with biotic or abiotic factors. Flowering plants have evolved a remarkable diversity of inflorescence branching patterns, which is largely governed by developmental decisions in inflorescence meristems and their derived meristems between maintenance of indeterminacy and commitment to the floral fate. Recent findings suggest that regulation of inflorescence architecture is mediated by flowering time genes, Arabidopsis LSH1 and Oryza G1 (ALOG) family genes, and the interaction between the auxin pathway and floral meristem regulators. In this review, we discuss how the relevant new players and mechanisms account for the development of appropriate inflorescence structures in flowering plants in response to environmental and developmental signals. Diverse inflorescence architectures in flowering plants During post-embryonic development of flowering plants, the shoot apical meristem (SAM) and root apical meristem (RAM) generate aerial and underground parts, respectively. The SAM gives rise to all aerial organs under a dynamic balance of growth and differentiation. It generates vegetative structures, such as leaves, stems, and axillary meristems, at the vegetative phase and is transformed into the main inflorescence meristem during the floral transition, when environmental and developmental conditions are optimal for plant reproductive success. The main inflorescence meristem either produces flowers or remains indeterminate to produce branch meristems, which could iterate the pattern of the main inflorescence meristem. Various branching patterns and the spatiotemporal generation of flowers from main and branch meristems contribute to a huge variety of inflorescence architectures observed in nature. The optimal inflorescence architecture plays a key part in reproductive success because it affects the ultimate number of flowers that set fruits and the competitive strength of plant individuals in interacting with biotic or abiotic factors, such as pollinators and wind [1–3].
Corresponding author: Yu, H. ([email protected]). 1360-1385/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2013.11.001
There are three major architectural types of inflorescences based on the termination events on the inflorescence meristems of various orders [4,5]. Plants such as Arabidopsis (Arabidopsis thaliana) develop the racemetype inflorescences, in which main inflorescence meristems grow indefinitely and generate either flowers or branch meristems that reiterate the pattern of the main inflorescence meristems (Figure 1). The panicle-type inflorescences are largely characteristic of grasses such as rice (Oryza sativa) and oat (Avena sativa). Main inflorescence meristems of these plants terminate after producing a series of lateral branch meristems, which eventually terminate in flowers after generating either flowers or higher-order branches (Figure 1). Unlike the racemeand panicle-type inflorescences, a cyme-type inflorescence, such as the one that develops in tomato (Solanum lycopersicum), lacks a main axis and terminates in a flower after generating a new inflorescence meristem that reiterates this pattern (Figure 1). In addition to the three architectural types and their variations, two basic growth habits, monopodial and sympodial, affect the diversity in inflorescence architecture. During the floral transition, the main SAMs of monopodial plants, such as Arabidopsis and rice, develop into the central leader inflorescence shoots while producing other subordinate branches. By contrast, the SAMs of sympodial plants, such as tomato, either terminate in reproductive structures or are aborted after a period of vegetative growth, and their growth continues from new axillary meristems that repeat this process. In tomato, the SAM terminates in a cyme-type inflorescence, and new vegetative growth continues from a sympodial shoot meristem produced from the axil of the youngest leaf [6–8]. The sympodial shoot meristem reiterates the pattern of the SAM to terminate in an inflorescence and initiate the generation of a new sympodial shoot meristem, eventually resulting in elaborate sympodial inflorescence shoots in tomato (Figure 1). Recent findings from different plant species have demonstrated that the integrated regulatory network that controls inflorescence architecture includes previously unrecognized components, such as flowering time genes and Arabidopsis LSH1 and Oryza G1 (ALOG) family genes, and an interaction between the auxin pathway and floral meristem regulators. In this review, we discuss how these new components contribute to the development of appropriate inflorescence architectures in flowering plants to ensure reproductive success under changing growth conditions. Trends in Plant Science xx (2013) 1–8
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Figure 1. Comparison of the inflorescence architecture of Arabidopsis, rice and tomato. (A) Schematic diagrams depicting the inflorescence structures of Arabidopsis, rice, and tomato. Brown circles, green arrows, and a green circle represent flowers, indeterminate shoots, and a determinate shoot, respectively. Black arrows indicate canonical axillary shoot meristems in tomato. (B) Sequential development of shoot meristems contributes to different inflorescence structures in Arabidopsis, rice, and tomato. In monopodial plants such as Arabidopsis and rice, during the floral transition the vegetative shoot meristem (VSM) is transformed into the main inflorescence meristem (IM) that subsequently generates all of the other branches and flowers. Arabidopsis develops the raceme-type inflorescence, in which a main IM grows indefinitely and generates either floral meristems (FMs) or primary branch meristems (pBMs) that reiterate the pattern of the main IM to produce either secondary branch meristems (sBMs) or FMs. In the panicle-type inflorescence of rice, the main IM terminates after the production of several pBMs that generate sBMs or spikelet meristems (SMs), each of which is transformed into a single FM. sBMs usually reiterate the pattern of pBMs to give rise to SMs and FMs. Tomato is a typical sympodial plant, in which the VSM terminates in a sympodial IM (SIM), whereas new vegetative growth continues from a sympodial shoot meristem (SYM) produced from the axil of the youngest leaf. The SYM reiterates the pattern of VSM to terminate in a SIM and initiate the generation of a new SYM. The SIM generates a new SIM before terminating in a FM, and reiteration of this pattern forms the cyme-type inflorescence in tomato.
Regulation of meristem identity determines inflorescence architecture Although a remarkable diversity of inflorescence architectures has evolved in flowering plants (Figure 1), the inflorescence branching pattern is mainly dependent on developmental decisions that take place in inflorescence meristems and their derived meristems; within each meristem, a decision is made between the maintenance of indeterminacy and commitment to the floral fate. Previous studies in Arabidopsis have suggested that an antagonistic interaction between the shoot identity gene TERMINAL FLOWER 1 (TFL1) and floral meristem identity genes, such as LEAFY (LFY) and APETALA1 (AP1), regulates the inflorescence branching pattern [9–11]. TFL1 is specifically expressed in the center of the main 2
inflorescence meristem and lateral branch meristems [10,12], whereas LFY and AP1 are strongly expressed in young floral meristems [13–16]. Loss of function of TFL1 results in early flowering and the conversion of the main inflorescence meristem and lateral branch meristems into floral meristems, which is accompanied with ectopic expression of LFY and AP1 in these meristems [9,17–19]. By contrast, the opposite phenotypes of late flowering and highly branched inflorescences are observable in transgenic plants overexpressing TFL1, in which upregulation of LFY and AP1 during the floral transition is delayed [12]. These results suggest that TFL1 activity is responsible for indeterminate growth of inflorescence meristems partly through preventing the meristems from acquiring the floral identity promoted by LFY and AP1. Conversely, floral meristem identity genes, such as LFY, AP1, and two AP1 homologs, CAULIFLOWER (CAL) and FRUITFULL (FUL), are required to repress TFL1 expression in floral meristems [10,11,19–21]. In the absence of these floral meristem identity genes, ectopic and/or upregulated expression of TFL1 contributes to the conversion of floral meristems into inflorescence shoots. Thus, TFL1 and floral meristem identity genes contribute to shaping the inflorescence architecture in Arabidopsis through antagonizing each other to determine the identity of inflorescence meristems and their derived meristems (Figure 2A). LFY encodes a plant-specific transcription factor, the orthologs of which are present as single-copy genes in most land plant species [22]. Although LFY-like genes share two highly conserved domains, their expression patterns and functions are diverse in various plants [23–27]. For example, unlike its counterpart in Arabidopsis, the rice ortholog of LFY, ABERRANT PANICLE ORGANIZATION 2/RICE FLORICAULA (Table 1), is not expressed in floral meristems and has a role in suppressing the transition from inflorescence meristems to floral meristems [28–30]. It has been proposed that LFY-like genes might have two functions: an ancestral role in promoting meristematic growth and a novel role in mediating floral identity [24]. These two functions might exist with different strengths under different regulatory contexts in most flowering plants, thus contributing to various inflorescence structures observed in nature. Whereas LFY-like genes occur in most land plants, AP1 orthologs belong to the euAP1 gene clade of MADS-box genes and are only present in the core eudicots that comprise the majority of extant angiosperm species [31]. The expression and function of AP1-like genes are usually related to flower development [4], whereas their functional modes differ in various plants. For example, AP1 is required for establishment of floral meristems in Arabidopsis, whereas the counterparts in rice, OsMADS14, OsMADS15, and OsMADS18 (Table 1), are involved in specifying inflorescence meristems rather than floral meristems [32]. TFL1 is a member of the CETS (CENTRORADIALIS, TFL1, and SELF-PRUNING) family proteins that have homology with highly conserved phosphatidylethanolamine-binding proteins (PEBPs) in eukaryotes [33,34]. So far, investigations on TFL1 orthologs in various plant species have shown that these genes have a relatively conserved role in affecting inflorescence architecture through preventing shoot meristems from differentiating
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Figure 2. Modulation of TERMINAL FLOWER1 (TFL1) expression determines inflorescence architecture. (A) Model for the regulatory network that determines inflorescence branching in Arabidopsis. The commitment of lateral branch meristems (BMs) from the inflorescence meristem (IM) to indeterminate shoots or determinate flowers contributes to the inflorescence branching pattern. In Arabidopsis, this developmental transition is determined by antagonistic interactions between the shoot identity regulator TFL1 and a group of regulators involved in mediating the acquisition of floral meristem (FM) identity, including LEAFY (LFY), APETALA1 (AP1), SHORT VEGETATIVE PHASE (SVP), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), AGAMOUS-LIKE 24 (AGL24), and SEPALLATA 4 (SEP4). The flowering time genes, SVP, SOC1, and AGL24, are suppressed by AP1 in emerging FMs, but their expression at appropriate levels in FMs is indispensable for AP1 to suppress TFL1 [38,56– 58]. SEP4 is suppressed by SVP, SOC1, or AGL24, but otherwise has a redundant role in suppressing TFL1 [38]. AP1 interacts with SVP, SOC1, AGL24, or SEP4 in vivo, and all of these MADS-box transcription factors bind to the overlapping 30 region of the TFL1 locus that is also associated with LFY [38,45]. LFY and AP1 promote mutual mRNA expression in FMs, whereas the auxin pathway induces LFY that in turn affects auxin biosynthesis, transport, and signaling [11,25,26,45,77], as illustrated in Figure 3. Arrows and T bars indicate promoting and repressive effects, respectively. The double-ended diamond arrow indicates a feedback regulation between LFY and the auxin pathway. (B) Comparison of the inflorescence architecture between an Arabidopsis wild-type (WT) plant (Columbia) and a tfl1 loss-of-function mutant. (C) Comparison of the inflorescence architecture between a WT (cv. Nipponbare) and a transgenic rice plant in which four rice RICE CENTRORADIALIS (RCN) genes are knocked down through RNA interference (RNAi).
into floral meristems (Figure 2B,C) [35–39]. Of the 19 known PEBPs in rice, four [RICE CENTRORADIALIS 1–4 (RCN1–4)] are closely related to TFL1 [40]. Overexpression of RCNs causes a late flowering and highly branching phenotype [37,41], whereas knocking down RCNs results in much smaller panicles with reduced branches in rice (Figure 2C) [38]. These observations, together with the studies on TFL1-like genes in various plant species [4], suggest that TFL1-like genes may have a general role in maintaining the indeterminacy of shoot meristems. In Arabidopsis, it has been proposed that TFL1 might antagonize another floral pathway integrator, FLOWERING LOCUS T (FT), to act as a transcriptional repressor through interacting with a bZIP transcription factor, FD, and negatively modulating FD-dependent transcription of downstream genes, including those involved in the regulation of floral meristem specification [42]. Many efforts have been made to understand the dynamic subcellular localization of TFL1 during Arabidopsis
development in order to elucidate the mechanisms by which TFL1 regulates downstream genes. Interestingly, experiments performed in several laboratories have obtained different and even opposite results, revealing TFL1 localization in a range of locations, including the cytoplasm, nucleus, and endomembrane compartments [42–44]. Because subcellular localization is essential for developmental regulators, such as TFL1, to exert their function, it is fundamentally important in future studies to address these discrepancies, which could be attributed to different antibodies and/or expression levels of the TFL1 protein in various experimental systems. Flowering time genes are important players in regulating inflorescence architecture Although it remains largely unknown how TFL1-like proteins affect downstream genes, intensive studies in Arabidopsis have provided significant insights into the regulation of TFL1 expression during the floral transition. 3
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Table 1. List of major genes that affect floral meristem identity and inflorescence architecture in Arabidopsis, and their orthologs in rice and tomato Arabidopsis gene TERMINAL FLOWER1 (TFL1)
Protein PEBP family protein
Function Maintains shoot identity
LEAFY (LFY)
Plant-specific TF
Promotes FM identity and floral organ patterning
APETALA1 (AP1)
MADS-box TF
Promotes FM identity and floral organ patterning
SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) AGAMOUS-LIKE 24 (AGL24); SHORT VEGETATIVE PHASE (SVP) SEPALLATA 4 (SEP4)
MADS-box TF
Mediates flowering time, FM specification, and floral organ patterning Mediates flowering time, FM specification, and floral organ patterning
OsMADS50; OsMADS56
Mediates flowering time, and FM and floral organ identity
MADS-box TF
MADS-box TF
Rice ortholog RICE CENTRORADIALIS1–4 (RCN1–4) ABERRANT PANICLE ORGANIZATION 2 (APO2)/RICE FLORICAULA (RFL) OsMADS14; OsMADS15; OsMADS18
Tomato ortholog SELF-PRUNING (SP)
Refs [9–11,17,18]
FALSIFLORA (FA)
[13–15,25,26,77]
MACROCALYX (MC); TM4; SLMBP7 (FUL2); SLMBP20 TM3; SLMBP14; SLMBP18
[16,19,38, 45,50,56]
OsMADS22; OsMADS47; OsMADS55
JOINTLESS; SLMBP24
[38,48,50,56–58]
OsMADS34
TM29; RIPENING INHIBITOR (RIN); TM5; LeMADS1; SLMBP21
[38,55]
[38,49,56,58]
Abbreviations: FM, floral meristem; IM, inflorescence meristem; PEBP, phosphatidylethanolamine-binding protein; SLMBP, SOLANUM LYCOPERSICUM MADS-BOX PROTEIN; TF, transcription factor; TM, TOMATO MADS-BOX.
Molecular genetic evidence suggests that AP1 and LFY are two upstream repressors of TFL1 in floral meristems [10,11,20,21]. Both AP1 and LFY are associated with an overlapping 30 region of the TFL1 gene, implying that they might interact to directly suppress TFL1 expression [45–47]. A recent study has revealed that a set of MADS-box transcription factors, namely SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), SHORT VEGETATIVE PHASE (SVP), AGAMOUS-LIKE 24 (AGL24), and SEPALLATA 4 (SEP4), act redundantly and directly to suppress TFL1 in emerging floral meristems [38] (Figure 2A). In the soc1-2 agl24-3 svp-41 sep4-1 quadruple loss-of-function mutant, the main inflorescence meristem continuously generates secondary and tertiary branch shoots, resulting in a massive inflorescence branching phenotype. Although AP1 and LFY are normally expressed in the anlagen of branch meristems in the mutant, they are unable to suppress the persistent expression of TFL1, which eventually confers shoot identity rather than floral identity on branch meristems. These observations indicate that SVP, SOC1, AGL24, or SEP4 is indispensable for the well-known function of AP1 and LFY in repressing TFL1. Chromatin immunoprecipitation and coimmunoprecipitation assays have shown that SVP, SOC1, AGL24, or SEP4 interacts with AP1 and directly binds to the 30 region of the TFL1 locus that overlaps with the region bound by both AP1 and LFY [38,45–47]. Among these four MADS-box transcription factors, SVP is a dominant regulator that suppresses TFL1 in wild-type inflorescence apices, whereas SOC1 and AGL24 exert similar repressive function in svp-41 mutants [38]. SEP4 is ectopically expressed in the inflorescence meristem of soc1-2 agl24-3 svp-41 mutants and acts as the main regulator for suppressing TFL1 only in the absence of SVP, SOC1, and AGL24. Thus, these MADS-box genes have redundant roles in regulating TFL1 expression in different genetic backgrounds. 4
SVP, SOC1, and AGL24 were first identified as important flowering time genes that regulate the floral transition in Arabidopsis [48–50]. SVP acts as a potent flowering repressor that interacts with another repressor, FLOWERING LOCUS C, to suppress the expression of two floral pathway integrators, FT and SOC1 [48,51,52]. By contrast, both SOC1 and AGL24 respond to multiple flowering genetic signals and interact with each other to promote flowering [49,50,53,54]. SEP4, which was first reported as a class E floral organ identity gene involved in the control of floral meristem and organ identity [55], also has a redundant role with other flowering promoters in regulating flowering (J. Liu et al., unpublished). Therefore, prior to their function in floral meristems, these genes are part of the regulatory network that determines the timing of the transition from vegetative to reproductive growth. In emerging floral meristems, the expression of SVP, SOC1, and AGL24 is downregulated by AP1 to appropriate levels to prevent the reversion of floral meristems into various shoot structures [56,57]. Expression of SVP, SOC1, and AGL24 at appropriate levels seems to have dual roles in this specific developmental context. On the one hand, they act redundantly with SEP4 to interact with AP1 to suppress the expression of the common target TFL1, thus eventually enabling the acquisition of floral identity in branch meristems [38]. On the other hand, SVP, SOC1, and AGL24 also directly repress the expression of SEP3, another class E floral organ identity gene that acts with LFY to activate class B and C gene expression, thus determining the timing of floral organ patterning by preventing premature differentiation of floral meristems into floral organs [58,59]. These results demonstrate a delicate mechanism through which SVP, SOC1, and AGL24 secure the development of a branch anlage into a transiently indeterminate meristem. This transient phase of indeterminacy not only prevents the branch meristem from reverting back to the shoot meristem but also permits the
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Review meristem to subsequently develop into a larger floral meristem containing sufficient cells for proper patterning of whorled organs by class B and C floral homoeotic genes. Taken together, SVP, SOC1, and AGL24 have crucial and persistent roles in mediating several successive developmental programs during the floral transition, including flowering time control, floral meristem specification, and floral organ patterning, all of which contribute to different extents to shaping the inflorescence architecture. Because the expression of SVP, SOC1, and AGL24 is tightly controlled by various environmental and developmental signals [48–52,54], the coordinated regulatory events mediated by these genes allow Arabidopsis plants to fine-tune the timing of flowering and subsequently develop appropriate inflorescence architectures for timely interaction with biotic or abiotic factors, thus ensuring the reproductive success under changing growth conditions. In rice, enhanced panicle branching with an increased number of higher order branches is observed [38] when the rice orthologs of SOC1 (OsMADS50 and OsMADS56) and SVP/AGL24 (OsMADS22, OsMADS47, and OsMADS55) (Table 1) are downregulated in the panicle phytomer2-1 ( pap2-1) mutant, in which a rice ortholog of SEP4, OsMADS34, is knocked out [60]. This phenotype, which is correlated with ectopic expression of RCN4 in these plants, resembles that exhibited by transgenic rice plants overexpressing RCNs [37,41]. These observations suggest that the interaction of flowering time genes with TFL1-like genes could be a conserved mechanism for regulating inflorescence architecture in dicots and monocots. ALOG family proteins mediate inflorescence architecture In addition to flowering time genes, ALOG family proteins, which are conserved in the plant kingdom with a single small domain of unknown function [61,62], have been recently demonstrated to play a part in mediating inflorescence architecture in both rice and tomato [8,63]. TAWAWA1 (TAW1) encodes one of the ten ALOG family proteins in rice and regulates inflorescence architecture through maintaining an indeterminate fate of inflorescence meristems and suppressing the specification of determinate spikelet meristems that later develop into floral meristems (Figure 1B) [63]. Downregulation of TAW1 causes early termination of inflorescence meristems and precocious formation of spikelet meristems, resulting in small inflorescences with a reduced number of primary branches in rice, whereas upregulation of TAW1 displays an increased branching phenotype because of its opposite effect on the regulation of inflorescence and spikelet meristems. Interestingly, the expression of rice orthologs of SVP (OsMADS22, OsMADS47, and OsMADS55) is upregulated by TAW1, whereas overexpression of OsMADS22 and OsMADS55 mimics the inflorescence phenotype caused by upregulation of TAW1, suggesting that TAW1 modulates inflorescence architecture partly through promoting SVP-like genes [63]. In contrast to SVP-like genes, genes involved in spikelet development, such as OsMADS7 (a SEP3 ortholog), OsMADS3, and OsMADS58 (orthologs of AGAMOUS, an Arabidopsis class C floral organ identity gene), are downregulated by TAW1. This repression could
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be similarly mediated by SVP-like genes, as demonstrated in Arabidopsis, in which SVP suppresses the expression of SEP3 and its downstream floral organ identity genes, including AGAMOUS, in floral meristems [58]. TERMINATING FLOWER (TMF) encodes another ALOG family protein and affects inflorescence organization in tomato [8]. Like TAW1 in rice, TMF maintains meristem indeterminacy and suppresses the adoption of floral fate in the meristem. In tmf loss-of-function mutants, the primary SAMs terminate as single flowers without formation of sympodial inflorescence meristems or vegetative shoot meristems. This is partially attributed to precocious activation of the F-box gene ANANTHA (AN), an ortholog of Arabidopsis UNUSUAL FLORAL ORGANS (UFO), and its transcription factor partner FALSIFLORA (FA), an ortholog of Arabidopsis LFY [8]. In addition, tomato orthologs of AP1 and SEP genes are upregulated in tmf. Thus, TMF affects inflorescence architecture in tomato possibly via preventing early expression of those genes that contribute to promoting floral fate. Whether this regulation is also mediated by SVP-like genes is so far unknown. LIGHT-DEPENDENT SHORT HYPOCOTYLS 3 (LSH3) and LSH4, also known as ORGAN BOUNDARY 1 (OBO1) and OBO4, encode two of the 11 ALOG family proteins in Arabidopsis [64,65]. Both LSH3 and LSH4 are expressed at the boundary of the SAM and lateral organs, which is similar to the expression pattern of TMF in tomato [8]. Ablation of the specific cells expressing LSH3 results in loss of the SAM and lateral organs. Constitutive expression of LSH3 and LSH4 generates ectopic meristems and chimeric floral organs in flowers [64,65]; this partially mimics the phenotype exhibited by mutations in UFO, a gene that shares overlapping expression patterns with LSH3 and LSH4, particularly at the boundary of the SAM [66,67]. Thus, the potential interaction between LSHs and UFO, which is analogous to the relationship between TMF and AN in tomato, could also regulate meristem maintenance and organogenesis in Arabidopsis. Knocking out LSH3 and LSH4 does not result in an obvious phenotype [64], and therefore it will be important to investigate other redundant factors, such as their interacting partners or other ALOG family proteins, to elucidate whether ALOG family proteins affect inflorescence architecture in Arabidopsis. In summary, accumulating evidence on the role of ALOG family proteins in maintaining meristem indeterminacy and suppressing floral identity, together with the unique expression pattern of LSH3, LSH4, and TMF in boundary regions of the SAM, indicates that ALOG family proteins might be an important group of regulators that affect inflorescence architecture through mediating the transition between undifferentiated and differentiated cells in the SAM. Auxin mediates floral initiation and inflorescence architecture Another essential question about inflorescence architecture, which is related to the above discussion on the regulation of meristem identity of lateral branches, is how the growth of branch meristems and their fate specification is 5
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YUC1 YUC4 TAR2 Auxin transport
PIN1 PID
Auxin biosynthesis
Auxin IAA1 IAA12/BDL IAA17 IAA29 MP/ARF5 LFY
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ANT AIL6
Iniaon of floral meristem TRENDS in Plant Science
Figure 3. The auxin pathway and LEAFY (LFY) interact to mediate the initiation of floral primordia. The auxin maximum at floral anlagen is required for the initiation of floral primordia and generated by polar auxin transport involving auxin efflux regulators, such as PIN-FORMED 1 (PIN1) and PINOID (PID) [68,69,71]. In incipient primordia, auxin induces LFY expression through triggering the degradation of INDOLE-3-ACETIC ACID 12/BODENLOS (IAA12/BDL), which physically interacts with and inhibits the activity of MONOPTEROS/AUXIN RESPONSE FACTOR 5 (MP/ ARF5), a protein that directly upregulates LFY and other two transcription factors, AINTEGUMENTA (ANT) and AINTEGUMENTA-LIKE6 (AIL6) [26]. LFY is involved in feedback regulation of the auxin pathway through negatively regulating the expression of several genes involved in auxin biosynthesis [such as YUCCA 1 (YUC1), YUC4, and TAR2] and promoting the expression of the auxin transport regulator PID and auxin signaling [25,26,46,47]. Promoting and repressive effects are indicated by arrows and T bars, respectively. Genes enclosed in colored boxes are transcription factors.
coordinated. Initiation of branch meristems with floral identity on the flanks of the inflorescence meristem is dependent on the auxin maximum at branch anlagen [68,69]. Loss-of-function mutations in the genes involved in auxin biosynthesis, the efflux carrier PIN-FORMED 1 (PIN1), and an AUXIN-RESPONSE FACTOR (ARF) gene MONOPTEROS (MP, also known as ARF5) all abolish floral meristem formation, resulting in naked inflorescence stems in Arabidopsis [70–72]. These observations indicate that auxin biosynthesis, transport, and signaling have an indispensable role in floral meristem initiation and inflorescence organization. Recent evidence has suggested that the interaction between LFY and the auxin pathway coordinates the outgrowth of primordia from the inflorescence meristem and the specification of their floral identity (Figure 3) [25,26]. Auxin activates MP by triggering the degradation of an AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) transcriptional repressor called IAA12/BODENLOS (BDL) that physically interacts with MP and suppresses its activity [26]. In incipient floral primordia, auxin-activated MP directly induces the expression of LFY and two AP2-like transcription factors, AINTEGUMENTA (ANT) and AINTEGUMENTA-LIKE6/PLETHORA3 (AIL6/PLT3) [26]. LFY has a pivotal role in specifying floral meristem identity [13,14], whereas ANT and AIL6 are essential for the growth of floral primordia [73–76]. Thus, auxin-activated MP coordinates fate specification and meristem growth during the initiation of floral primordia. It is noteworthy that LFY is also involved in feedback regulation of the auxin pathway through modulating expression of genes involved in auxin biosynthesis, transport 6
and signaling (Figure 3) [25,26,46,47]. LFY is physically associated with many genes in the auxin pathway [46,47], implying that LFY could directly control the transcription of these genes. Expression analyses have revealed that LFY downregulates several genes involved in auxin biosynthesis, such as YUCCA 1 (YUC1), YUC4, and TRYPTOPHAN AMINOTRANSFERASE RELATED 2 (TAR2) [25], but upregulates the auxin transport regulator PINOID (PID) [26]. In agreement with these expression data, auxin levels are reversely correlated with LFY activity in inflorescence apices [25], whereas LFY promotes auxin accumulation in floral primordia [26]. Furthermore, LFY affects the expression of AUX/IAA genes, such as IAA1, IAA17, and IAA29, and upregulates the expression of the auxin-response reporter DR5rev::3XVenus-N7 or DR5rev::GFP in floral meristems [25,26], indicating that LFY also positively regulates auxin signaling. Positive and negative feedback regulation of auxin biosynthesis, transport and signaling by LFY provides pivotal mechanisms for coordinate and subtle regulation of several successive developmental programs required for the establishment of floral meristems and the resulting inflorescences. Although the heterogeneous distribution of auxin at floral anlagen is important for initiation and growth of primordia, timely induction of LFY by auxin in the primordia not only determines the specification of floral meristem identity but also modulates the auxin level and distribution in developing floral meristems, which is required for subsequent initiation and patterning of various floral organs. Therefore, the interaction between LFY and the auxin pathway integrates auxin signaling into the regulatory network that determines inflorescence branching in Arabidopsis (Figure 2A). Concluding remarks Sustained efforts of many laboratories over the past few years have provided significant insights into the regulation of inflorescence architecture that determines plant reproductive success. Newly recognized components of this regulatory event in various plants species include a set of flowering time genes that have essential roles in coordinating flowering time and subsequent floral meristem development, and ALOG family genes that regulate the meristem identity in the shoot apex. Furthermore, interaction and feedback regulation between the auxin pathway and LFY mediate the initiation and specification of floral meristems, forming an integral part of the regulatory hierarchies required for shaping inflorescence architecture in Arabidopsis. These advances, however, raise further questions that need to be addressed. For example, the interaction between ALOG family proteins and other known floral meristem regulators is still largely unknown. Also, it would be interesting to investigate whether the auxin pathway interacts with other conserved regulators in floral meristems because the functions of LFY orthologs are diverse in flowering plants. We can expect to observe more intertwined feedback loops and new players in the regulation of inflorescence architecture through addressing these questions. Acknowledgments The preparation of this review was supported by the Academic Research Fund (MOE2011-T2-2-008) from the Ministry of Education, Singapore,
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Review the Singapore National Research Foundation under its Competitive Research Programme (NRF2010NRF-CRP002-018), and the intramural resource support from National University of Singapore and Temasek Life Sciences Laboratory. We apologize to those authors whose excellent work could not be cited owing to space limitations.
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