The Maize Leaf - Cell Press

Opinion

The Maize Leaf: Another Perspective on Growth Regulation Viktoriya Avramova,1,z Katrien Sprangers,1,z and Gerrit T.S. Beemster1,* The Arabidopsis thaliana root tip has been a key experimental system to study organ growth regulation. It has clear advantages for genetic, transcriptomic, and cell biological studies that focus on the control of cell division and expansion along its longitudinal axis. However, the system shows some limitations for methods that currently require too much tissue to perform them at subzonal resolution, including quantification of proteins, enzyme activity, hormone, and metabolite levels and cell wall extensibility. By contrast, the larger size of the maize leaf does allow such analyses. Here we highlight exciting new possibilities to advance mechanistic understanding of plant growth regulation by using the maize leaf as a complimentary system to the Arabidopsis root tip.

Trends The recent development of new molecular techniques led to opportunities to study organ growth regulation (through the effects on cell division and cell expansion) at different organizational levels. The Arabidopsis root tip is currently the best-studied model system in organ growth research, being particularly suitable for genetic, transcriptomic, and cell biology studies. The maize leaf growth zone offers unique possibilities for systems biology of organ growth at subzonal resolution, including measurements of metabolites, proteins, enzyme activities, and cell wall extensibility.

Model Systems to Study Organ Growth Regulation How plants regulate the growth of their organs has been a central theme in plant research from its early days [1]. Plant organ growth is the result of the combined activity of two cellular processes, division and cell expansion. To study these processes, various model organs have been used. Hypocotyls are particularly suitable for cell expansion studies since their growth depends solely on this process [2]. By contrast, the apical regions of axial plant organs, such as roots and stems, and the basal parts of monocot leaves represent ideal model systems for quantitative studies of the spatial patterns of both cell division and cell expansion. Conceptually, they can be treated as 1D, steady-state systems in which cell proliferation (see Glossary) and cell expansion occur as a gradient along the axis [3] jointly determining overall growth, which is a useful simplification in growth studies. Knowledge about how these cellular processes are regulated has rapidly accumulated over the past decades, aided by the introduction of A. thaliana as a model organism. Besides its genetic advantages, its small size and simple anatomy and the fact that it can be easily grown in media made it attractive for basic research [4]. However, this size advantage also limits its possibilities to genetic, transcriptomic, and cell biology research. For studies at other organizational levels (proteome, metabolome, enzyme activities, physiology) the organs are too small. By contrast, the maize (Zea mays L.) leaf growth zone has division and expansion zones spanning several centimeters [5], compared with fractions of a millimeter in the Arabidopsis root tip [6], providing enough tissue for analyses with high resolution at all organizational levels. Therefore, combining the advantages of both models would contribute to more integrated knowledge about organ growth regulation. Roots and monocot leaves perform different functions and their development is adapted to contrasting heterogeneous environments. Nevertheless, comparing studies in the two systems reveals remarkable similarities between the underlying cellular processes and associated molecular growth regulatory mechanisms. Hence, combining knowledge from the two systems

Trends in Plant Science, December 2015, Vol. 20, No. 12

1

Molecular Plant Physiology and Biotechnology, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium

*Correspondence: [email protected] (G.T.S. Beemster). z These authors contributed equally and should be considered co-first authors.

http://dx.doi.org/10.1016/j.tplants.2015.09.002 © 2015 Elsevier Ltd. All rights reserved.

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Box 1. Similarities and Contrasts between the Arabidopsis Root Tip and the Maize Leaf in Terms of Hormones and ROS Localizing the action and distribution of hormones and ROS along the growth zone of Arabidopsis roots and maize leaves reveals a pattern of activity/concentration peaks that coincides with the developmental zones (Figures 1 and 2). Comparing the specific patterns for individual hormones between the two model systems shows both similarities and contrasts (potentially indicating organ-specific aspects of developmental regulation). For instance, BR is active in the division zone of both Arabidopsis root tips and maize leaves. Also, the activity of IAA in the division zone of Arabidopsis roots resembles the distribution in the maize leaf, whereas the pattern in the elongation zone is opposite. A clear peak in the transition zone is formed by different hormones (CK for Arabidopsis root, GA for the maize leaf). For GA, CK, and ABA, there is no obvious correlation between the distribution pattern in maize leaves and the localization of activity in Arabidopsis roots. The distribution pattern of a hormone might, however, not colocalize with its activity map, so the differences that are observed might be due not only to organ-specific aspects. In terms of ROS (especially H2O2), there seems to be no correlation in distribution between the two organs, which might indicate more organ-specific regulation. However, within the maize leaf the concentration of H2O2 fits the activity of the corresponding enzymes.

would allow us to augment our understanding about the common principles of leaf and root development as well as organ-specific aspects (Box 1). In this opinion article we compare the technical possibilities and limitations of both models to define to what extent they can complement each other for systems biology approaches aimed at a better understanding of plant organ growth regulation.

Cell Level Given the central role of the cell division and expansion processes in organ growth regulation, a first step in a systems approach to understand (differences in) whole organ growth rates is a proper analysis of both processes in relation to their position along the root/leaf axis. Kinematic analysis provides a rigorous framework for these quantifications [7] and the development of new software makes it increasingly feasible to perform [3]. The Arabidopsis root has been used extensively in kinematic growth analyses to study the contribution of cell division and cell expansion to organ growth [6]. The ability to grow these roots on agar media allows direct time-lapse observation of tissue movement velocity along the root axis and its limited diameter (approximately 140 mm [8]) allows cell length measurements on whole mounted roots. Both measurements can be combined to calculate cell division rates and to determine the boundaries between the proliferation, elongation, and mature zones [6]. Alternative methods to identify the transition between proliferation and expansion are localization of the inflection point in the cell length profile [9], the use of cell cycle marker lines [10], and cell wall and vacuole viability staining [11]. In maize, growing leaves are surrounded by older ones, which prevents velocity measurements. Kinematic analysis of the maize leaf has therefore been adapted, combining measurements of leaf elongation rate, cell length profile, and the localization of mitotic cells after DNA staining [7]. Cell cycle marker lines, however, are not available in this species and cytochemical staining has to our knowledge not been used to determine meristem size, so the toolbox is more limited.

Hormonal Regulation Plant hormones such as auxin [indole-3-acetic acid (IAA)], cytokinins (CKs), gibberellins (GAs), brassinosteroids (BRs), and abscisic acid (ABA) have long been recognized as endogenous regulators of cell division and expansion and plant development. Each one regulates these processes in a specific manner and whole-organ growth depends on their crosstalk [12]. Various methodologies have been developed to study hormones and their effect on root growth in Arabidopsis. First, the use of mutants of hormone-related target genes, often combined with external application of hormone precursors and/or synthesis inhibitors, provides a powerful

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Glossary AUX: auxin influx carrier. Cell proliferation: the process of cell division combined with cell growth [56]. DELLA mechanism: DELLA is a family of proteins that act as negative regulators of downstream GA signaling. In the absence of GA, DELLA inhibits the gene expression of GA-responsive genes. When GA is present, it binds to its receptor GID1 and this results in changes in protein conformation so that the complex GID1–GA–DELLA is formed, resulting in the degradation of DELLA via the ubiquitin–proteasome pathway and enabling the expression of the GA-responsive genes. DII–VENUS reporter system: this reporter system uses fluorescence to visualize auxin distribution. The reporter is constitutively expressed and comprises the auxin-binding domain (DII) of auxin/IAA proteins and a fast-maturating variant of the YFP VENUS. Auxin triggers the degradation of the reporter; therefore, the absence of fluorescence indicates the presence of auxin. Jas9–VENUS reporter system: this reporter system uses the same principle as the DII–VENUS construct to visualize jasmonate distribution. Jas9 is a motif in jasmonate–ZIM domain (JAZ) proteins responsible for jasmonate-dependent degradation. Kinematic analysis: provides a mathematical framework to quantify cell division and cell expansion rates to define to what extent both processes contribute to growth differences at the whole-organ level. Omics: a generalized term that includes all biological disciplines ending in ‘-omics’ (e.g., genomics, transcriptomics, proteomics, metabolomics). All of these disciplines aim to describe the structure, function, and dynamics of a biological system by characterizing and quantifying subsets of molecules (e.g., transcripts, proteins, metabolites). PINs: a class of auxin efflux carriers.

Box 2. Mapping Hormone Responses in the Arabidopsis Root Tip Tissue-specific marker lines were used for flow sorting of the major cell types as a function of position along the root axis, followed by genome-wide expression analysis. Hormone responses were determined by the expression profiles of known response genes to specific hormones. The activity of auxin was located in the elongating stele while GA activity was mapped in the cortex, endodermis, and stele of the transition zone. JA-related expression patterns were detected in the lateral root cap and epidermis of the meristem and transition zone [19]. In addition, the development of tissue-specific expression systems driving the expression of dominant-negative regulators of hormone response allowed the mapping of hormone responses in regulating root growth [57,58] (Figure 1). In contrast to what was suggested by the geneexpression patterns, GA function was limited to the endodermis with no differences detected at a subzonal level. Auxin function was limited to the elongating epidermal cells and quiescent center (QC), but also to a lower extent in the stele along the whole root growth zone. In addition, CKs targeted all tissues in the transition zone, whereas ABA affected QC cells only and the epidermis of the proliferation zone was reported as the primary responsive tissue for BRs [57,58].

approach to study the role of plant hormones during root growth [13,14]. Determination of hormone distribution down to the level of individual cell types was enabled by the development of reporter systems such as the DII–VENUS [15] and Jas9–VENUS [16] constructs for auxin and jasmonic acid (JA), respectively, and by the use of bioactive fluorescent hormone analogs [17,18]. By combining transcriptome analysis, reporter constructs, and mutants it has been possible to explain the spatial distribution of auxin based on the expression and polarity of auxin transporters including PINs and AUXs [19–21]. Moreover, based on tissue-specific expression systems and flow sorting of tissue-specific marker lines it was possible to construct a detailed hormone action map (Box 2). Despite the wealth of available tools, the Arabidopsis root has limitations. Reporter systems do not exist for all hormones. Moreover, they visualize the transcriptional response, which may not directly reflect the concentrations of active compound. The quantification of IAA levels in all cell types of the Arabidopsis root tip was achieved by combining fluorescence-activated cell sorting (FACS) and mass spectrometry [22], but the obtained data do not allow determination of the spatial distribution of the IAA gradient across the developmental gradient. A more recent experiment shows the possibility of analyzing most of the known IAA precursors and degradation products in a relative small amount of plant tissue (approximately 20 mg [23]). However, if this kind of analysis were performed at a subzone level, the amount of root tips needed would be extremely high (Table 1). Although these experiments show the possibility of quantifying this specific hormone, to our knowledge subzone quantification in the Arabidopsis root has not been performed for other hormones or hormone intermediates, probably because of the amount of material required (Table 1). For the maize leaf, the genetic resources are more limited. No tissue-specific marker lines are available, but limited hormone mutants exist [24,25] and reporter lines have been developed only for auxin [26,27]. However, the larger size of the maize leaf allowed the quantification of IAA, CKs, the BR castasterone, ABA, JA, and salicylic acid at subzonal resolution by mass spectrometry, while for GA, in addition to the bioactive GA1 and 4, most biosynthetic and catabolic intermediates were measured [24] (Figure 1 and Box 1).

Reactive Oxygen Species (ROS) Homeostasis The balance of ROS also regulates meristem size. In the Arabidopsis root, ROS distribution was analyzed indirectly by staining techniques [28]. Superoxide (O2) is concentrated in the meristematic zone, where it promotes cell proliferation. By contrast, hydrogen peroxide (H2O2) amounts are higher in the elongation zone, promoting cell elongation (Figure 2). In addition to staining, the spatial distribution of ROS in the maize leaf can be determined on extracts by means of spectrophotometry [29] (Figure 2). The amount of tissue that the maize leaf provides enables direct measurements of H2O2 [30] and even biochemical activity


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Table 1. Comparison between Minimal Number of Arabidopsis Roots and Maize Leaves in Terms of Required Tissue for Various Analysesa Analysis

Method

Plant Tissue Required

Minimal Number of Arabidopsis Roots

Minimal Number of Maize Leaves

Meristem (500 mm)

Growth Zone (1850 mm)

Meristem (1.5 cm)

Growth Zone (10 cm)

Refs

Transcriptomics Microarray

50–100 mg (50–200 mg total RNA)

6714

2414

1

1

[59]

Microarray (cDNA tag target amplification)

0.5 mg (0.1 mg total RNA)

67

24

1

1

[59]

Microarray (protoplasting)

5000 seeds per replicate 10 000 000 cells

5000

5000

NDo

ND

[19,42]

RNA-seq

50–100 mg (4 mg total RNA)

6714

2414

1

1

[60]

2D gels

200 mg

26 858

9657

4

1

[61]

30 mg to 1 g (100 mg protein)

4029

1449

1

1

[27,44]

Proteomics

LC –MS b

c

Enzyme activity Fructan metabolism

HPLCd on a cation exchange column + pulsed amperometric detector

1g

134 289

48 285

22

2

[62]

Antioxidant enzymes

Colorimetric plate assays

100 mg

13 429

4828

2

1

[63]

IAA

GCe–MS

1 mg

134

48

1

1

[64]

IAA intermediates

One-step SPEf purification (LC–MRMg–MS)

20 mg

2686

966

1

1

[23]

CKs

LC–(+)ESIh–MS–MS

50 mg

6714

2414

1

1

[65]

LC–FABi–MS

250 mg

33 572

12 071

5

1

[66]

LC–singlequadrupole MS

1g

134 289

48 285

22

2

[23]

GC–MS

1 mg

134

48

1

1

[67]

Hormones

GAs + intermediates

GC–MS

20 g

2 685 772

965 692

435

47

[68]

GC–MS/SIMj

271 g

36 392 209

13 085 124

5900

633

[69]

UHPLC –MS/MS

20 mg

2686

966

1

1

[70]

LC–MS/MS

100 mg

13 429

4828

2

1

[71]

GC–MS

500 mg

67 144

24 142

11

1

[72]

Trehalose

LC–triplequadrupole MS

12 mg

1611

579

1

1

[73]

Glucose, fructose, and sucrose

HPLC

800 mg

107 431

38 628

17

2

[74]

BRs

k

ABA

Metabolites

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Table 1. (continued) Analysis

Method

Plant Tissue Required

Minimal Number of Arabidopsis Roots

Minimal Number of Maize Leaves

Meristem (500 mm)

Growth Zone (1850 mm)

Meristem (1.5 cm)

Growth Zone (10 cm)

Refs

Glucose, fructose, sucrose, and iminosugars

LC–MS

500 mg

6714

2414

1

1

[75]

Minerals (Ca, K, Mg, Na, N, and P)

Inductively coupled plasma emission spectrometry

100 mg (dry weight)

124 619 041

67 628 801

20

3

[76]

Antioxidants

Colorimetric plate assays

100 mg

13 429

4 828

2

1

[63]

Hydrogen peroxide

Spectrophotometry by potassium iodide

250 mg

33 572

12 071

5

1

[29]

MDAl

TCAm/TBAn reaction

250 mg

33 572

12 071

5

1

[29]

Glutathione, ascorbate, proline

HPLC

100 mg

13 429

4 828

2

1

[63]

a

For calculations see supplemental information online. LC, liquid chromatography MS, mass spectrometry d HPLC, high-performance liquid chromatography e GC, gas chromatography f SPE, solid-phase extraction g MRM, multiple reaction monitoring h ESI, electrospray ionization i FAB, frit-fast atom bombardment j SIM, selected ion monitoring k UHPLC, ultra-high-pressure liquid chromatography l MDA, malondialdehyde m TCA, trichloroacetic acid n TBA, thiobarbituric acid o ND, not defined. b c

measurements of the main redox enzymes regulating ROS concentration [31] (Figure 2 and Box 1).

Cell Wall Properties As turgor is typically invariant across the growth zone of growing organs [32], cell elongation depends on the mechanical properties of the cell wall [33]. The cell wall mechanical properties of Arabidopsis roots have been poorly examined. To our knowledge, only plasticity measurements have been performed to investigate the cell wall extensibility of Arabidopsis in the elongation zone [34]. However, specific zones have recently had their cell wall epitopes profiled using a panel of antibodies and sugar-binding proteins [35]. Cell growth is regulated by the action of wall-modifying enzymes such as xyloglucan endotransglycosylases/hydrolases (XTHs) [36]. An in vivo study showed that xyloglucan endotransglycosylase (XET) activity and its donor substrate colocalize in the elongation zone of Arabidopsis roots [36]. The zone-specific quantification of extractable enzyme activity in vitro, however, is limited due to the small size of the root. In maize leaves extensibility measurements of epidermal peels (length, 3 cm; width, 1.0 cm) are feasible using linear variable differential transducers [37], which offers the possibility of


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IAA QC + epidermis

GA endodermis

CK all ssues

BR

Transcript abundance

(B)

Tissue specific expression system

(A)

IAA stele

GA endodermis, cortex, stele

JA lateral root cap, epidermis

epidermis

ABA QC

Key:

D

T

E

Proliferang cells

M

Expanding cells Mature cells

(C)

Key:

High

GA IAA CK BR ABA - JA - SA Low

Figure 1. Comparison of Hormone Distribution along the Growth Zone between the Arabidopsis Root and the Maize Leaf. (A,B) Tissue-specific hormone-action map along the growth zone of the Arabidopsis root, based on tissue-specific expression systems [57,58] (A) or transcript abundance [19] (B). (C) Hormone concentrations along the maize leaf growth zone [24]. Abbreviations: ABA, abscisic acid; BR, brassinosteroid; CK, cytokinin; D, division zone; E, elongation zone; GA, gibberellin; IAA, auxin; JA, jasmonic acid; M, maturation zone; SA, salicylic acid; T, transition zone.

performing zone-specific extensibility measurements. The large size of the maize leaves also allows sampling at subzone resolution of adequate tissue for enzyme extraction [38].

Metabolite Levels Metabolites such as sugars (e.g., hexoses, trehalose) and minerals (e.g., nitrates, phosphates) are essential for organ growth regulation. For tissue sampling with adequate resolution through the growth zone of the Arabidopsis root tip, microdissection is needed, resulting in sample volumes insufficient to conduct nutrient or mineral quantification. For some metabolites

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(A)

H2O2 O2–

Key:

D

T

E

Proliferang cells

M

Expanding cells Mature cells

(B)

High

Key: SOD POX CAT NOX H2O2

Low

Figure 2. Comparison of Redox Regulation along the Growth Zone of the Arabidopsis Root and the Maize Leaf. (A) Distribution of hydrogen peroxide (H2O2) and superoxide (O2) along the Arabidopsis root growth zone [28]. (B) Activity of the main redox-regulating enzymes and H2O2 concentration along the maize leaf growth zone [31]. Abbreviations: CAT, catalase; D, division zone; E, elongation zone; M, maturation zone; NOX, nicotinamide adenine dinucleotide phosphate oxidase; POX, peroxidase; SOD, superoxide dismutase; T, transition zone.

(e.g., sucrose, hexose) small amounts of tissue (1 mm) suffice [39] but for others (e.g., minerals) most studies have been conducted on whole-root samples [40], probably because of tissue limitations (Table 1). The determination of metabolite concentrations is much easier in long growth zones where there is no need to pool many samples (Table 1). Concentrations of inorganic and mineral nutrients have been measured across the growth zone of developing maize leaves showing different distribution patterns of ion density (K, Cl, Ca, Mg, P [41]).

‘Omics’ Studies The availability of the Arabidopsis genome sequence allowed the development of genome-wide microarrays. Using these in combination with flow sorting of marker lines expressing GFP in specific cell types made it possible to construct maps of cell-type-specific gene-expression profiles as a function of position along the root developmental gradient [19,42]. Maps like these


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are useful for assessing the function of genes involved in organ growth and development. However, it is well known that for many genes there is no strong correlation between mRNA levels and protein activity, due to translational control, proteolysis, secondary protein modifications, and complex formation. It is clear that detailed understanding of the regulation of biological processes can be obtained only by studying transcriptome, proteome, metabolites, and protein (enzyme) activities simultaneously and in the same experimental system (see Outstanding Questions). The small size of the Arabidopsis root, however, limits the spatial analysis of gene function to the transcriptome level. Since the maize genome has been sequenced, zone-specific transcriptome [43] and proteome [44] studies have been conducted. Interestingly, mRNA and protein abundance showed significant positive correlations but to differing extents across the developmental gradient [45]. Moreover, a parallel proteome and phosphoproteome study has demonstrated the importance of post-translational modifications in the developmental transitions along the maize leaf axis [27].

Modeling Modeling is a tool that enables the integration of current knowledge toward a systems-level understanding of the complex behavior of a biological system. A recent review describes the currently available modeling tools used to model cell division and expansion in multicellular organisms [46]. The central role of the classical hormones in these processes forms the basis for simulation models of root growth regulation [20,47]. Integrated systems analysis, based on PIN distribution in the Arabidopsis root tip, yielded a map of auxin fluxes and distribution in the growth zone, visualizing the dynamics of auxin transport along the root axis [20]. After unraveling the molecular basis of GA action [48] and defining its distribution in root tissues by fluorescent labeling [17], the sites of this action were also mapped along the Arabidopsis root axis [49], helping us to understand how this hormone regulates organ growth. Models of the combined action of other hormones controlling the auxin gradient explain the importance of plant hormone crosstalk in the regulation of root growth [50]. Additionally, mechanical modeling shows how cell properties and shapes contribute to tissue extensibility and how intercellular signals regulate cell expansion through controlled changes in cell wall stiffness in the elongation zone [32]. Although the modeling tools would essentially be the same for the maize leaf, developmental models integrating molecular and cellular data with our knowledge have not been developed for this model system (see Outstanding Questions).

Concluding Remarks and Future Perspectives The development of mechanistic simulation models of growth of the Arabidopsis root illustrates its current leading position as a model system. Significantly more knowledge has been acquired compared with other plant model systems with similar characteristics, including the maize leaf. However, as we have shown, inspired by these studies in Arabidopsis very similar studies can be conducted in the maize leaf, allowing us to quickly bridge this knowledge gap. Moreover, our analysis of the methods available to date and the amount of tissue required to perform them (Table 1) clearly show the limitations of the Arabidopsis root tip for studies of other regulatory levels, including the quantification of proteins, enzyme activity, hormone and other metabolite levels, and cell wall extensibility. Clearly such studies are needed to advance our understanding of growth regulatory mechanisms. Therefore, we propose that the maize leaf, with a similar spatiotemporal gradient of cell division and expansion but a much larger size, could serve as a valuable model system to complement the Arabidopsis root tip. Moreover, its size also facilitates exciting new experimental approaches that could be developed in this system to take organ growth research to a new level.

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Outstanding Questions How do different organizational levels interact in the regulation of plant organ growth? Can we define common organ growth regulatory principles and organ-specific variations by combining information from the two model systems (Box 1) and use those to build realistic mechanistic simulation models? How is cell wall extensibility regulated in the individual developmental zones by different enzymes and other growth regulatory substances (e.g., hormones, sugars)? Which growth-regulating processes are affected by the various environmental stressors (e.g., drought, heat, pathogens)? How can we improve growth under these conditions?

The measurements of cell wall extensibility can be combined with adding growth regulatory

substances to different parts of the growth zone and testing their functionality (see Outstanding Questions). For example, exogenous addition of XTHs to growing Arabidopsis seedlings has an inhibitory effect on root elongation as a whole [51]. The maize leaf offers the opportunity to apply XTH or other enzymes (e.g., expansin, pectin lyase, peroxidase) to subzonal segments dissected from the growth zone and measure their effect on cell wall extensibility and hence cell growth. Similar experiments could be performed with other growth regulatory substances (hormones, sugars [52]). Although metabolite levels are of regulatory importance, understanding how their spatial distribution is established requires determining accumulation rates, which are the result of synthesis, import, degradation and/or export, and dilution by growth. Combining spatial patterns of growth velocity with metabolite concentrations along the growth zone enables the determination of metabolite deposition rates [53], providing a basis to link metabolite distributions with enzyme activities. Ultimately, knowledge generated by plant scientists should find its way toward applications of societal relevance. Although the molecular basis of some beneficial crop characteristics have been elucidated with the help of findings in Arabidopsis (e.g., the DELLA mechanism of GA-regulated organ growth [54,55]), working directly on a crop narrows the gap between laboratory and field (see Outstanding Questions). Acknowledgments This work was supported by a PhD fellowship of the University of Antwerp to V.A., a PhD fellowship from the Flemish Science Foundation (FWO, 11ZI916N) to K.S., project grants from the FWO (G0D0514N), a concerted research activity (GOA) research grant, ‘A Systems Biology Approach of Leaf Morphogenesis’, from the research council of the University of Antwerp, and the Interuniversity Attraction Poles (IUAP VII/29, MARS) ‘Maize and Arabidopsis Root and Shoot Growth’ from the Belgian Federal Science Policy Office (BELSPO) to G.T.S.B.

Supplemental Information Supplemental information associated with this article can be found, in the online version, at doi:10.1016/j.tplants.2015.09. 002.

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