Review

Tansley review Molecular basis of angiosperm tree architecture Author for correspondence: Chris Dardick Tel: +1 304 725 3451 Email: [email protected]

Courtney A. Hollender and Chris Dardick Appalachian Fruit Research Station, Agricultural Research Service, United States Department of Agriculture, 2217 Wiltshire Rd, Kearnysville, WV 25430, USA

Received: 25 June 2014 Accepted: 30 October 2014

Contents Summary

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I.

Introduction

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V.

Conclusions

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Acknowledgements

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Components of tree architecture

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References

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III.

Tree architecture categorizations

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IV.

The molecular basis for non-standard tree architectures

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Summary New Phytologist (2015) 206: 541–556 doi: 10.1111/nph.13204

Key words: compact, dwarf, growth habits, pillar, shoot architecture, tree genetics, weeping.

The architecture of trees greatly impacts the productivity of orchards and forestry plantations. Amassing greater knowledge on the molecular genetics that underlie tree form can benefit these industries, as well as contribute to basic knowledge of plant developmental biology. This review describes the fundamental components of branch architecture, a prominent aspect of tree structure, as well as genetic and hormonal influences inferred from studies in model plant systems and from trees with non-standard architectures. The bulk of the molecular and genetic data described here is from studies of fruit trees and poplar, as these species have been the primary subjects of investigation in this field of science.

I. Introduction Trees can be broadly defined as perennial woody plants with a prominent primary shoot, or trunk, from which lateral branches emerge. Tree forms have repeatedly evolved throughout evolutionary history and do not constitute a single clade or group of plants (Groover, 2005). Both the low-growing herbaceous strawberry and the apple tree are members of the Rosaceae family despite their radically different structures, whereas structurally similar sweet gum and maple trees are members of different orders (Saxifragales and Sapindales, respectively). Therefore, it seems likely that tree form repeatedly arose through changes in conserved genetic, molecular and hormonal pathways. Deciphering the origins of tree forms and the biology behind their development could lead to significant advances in orchard and forestry industries. This review covers basic concepts of tree architecture, as well as No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

known molecular and genetic mechanisms associated with the determination of tree architecture. The architecture of the aboveground portion of a plant is highly complex. It is the sum phenotype of multiple parameters including, but not limited to, overall height, the pattern and periodicity of branching, and the size, growth angle and orientation of each branch. Trees have a high degree of plasticity and adjust their structures in response to environmental stimuli, such as light, nutrient availability and crowding (Tomlinson, 1983), yet their genetic make-up substantially constrains spatial and temporal growth patterns (Halle et al., 1978; Mehlenbacher & Scorza, 1986; Scorza et al., 2002; Barthelemy & Caraglio, 2007; Busov et al., 2008). Although the molecular and genetic details regarding tree development are not well known, new advances in genomics and associated tools are now enabling researchers to tackle questions in what have been historically intractable organisms for genetic New Phytologist (2015) 206: 541–556 541 www.newphytologist.com

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research. These new technologies are fueling excitement among both industry and researchers in the light of the tremendous possibilities to achieve radical improvements in tree-based industries. The importance of plant architecture was demonstrated during the green revolution by the selection of rice and wheat plants with short, sturdy stalks and upright tillers. These architecturally modified plants could be planted at higher density and support greater grain weights, thus enabling greater food production (Peng et al., 1999; Hedden, 2003). In maize, selection for increased apical dominance and reduced tillering led to early improvements over its teosinte ancestor. Since the 1930s, maize density has grown from 30 000 to over 80 000 plants per hectare (Duvick, 2005). These improvements are a result of beneficial architectural changes. More upright leaf angles relative to the midrib promote efficient light capture under crowded conditions (Pendleton et al., 1968). Breeding for superior shoot architectures could likewise revolutionize tree crop industries. Ideal architectures for fruit and nut trees could include semi-dwarf statures as well as trees with fewer and shorter branches. Such trees have the potential to increase productivity via higher density plantings and reduced management, resulting in reduced land, water, pesticide and fertilizer use (Scorza et al., 1999; Scorza, 2005). In addition, the ability to manipulate and reduce overall tree size, reduce branch number and specify branch orientation could minimize pruning and maximize light penetrance. Architectures that more easily facilitate mechanized fruit thinning and harvesting could also be developed. Principles for forestry species may differ, but would still involve similar growth parameters, including alterations in growth rate, branch numbers, wood chemistry and branch orientation. Thus far, comparatively limited progress has been made in breeding for improved tree architectures. Such efforts are hampered by the large size of trees and their long generation times. Multifarious efforts in diverse tree species are working towards speeding up the development of useful architectures in commercial tree crops (Scorza, 2005). In an effort to aid the selection of ideal architectures early on in the breeding process, quantitative trait locus (QTL) analysis has been performed for internode length, tree height and geometry, and aspects of branching in apple, spruce, rubber and poplar, among other species (Zhang et al., 2006; Kenis & Keulemans, 2007; Segura et al., 2007, 2008; Prunier et al., 2013; Souza et al., 2013). Although QTLs can provide useful molecular markers for the early selection of desired traits by breeders, they do have limitations. QTLs are often specific to their species of origin, if not solely the genetic background of the cultivars they were generated from. Therefore, the identification and functional characterization of genes that contribute to specific aspects of tree architecture will be critical to fully exploiting tree genomes for crop improvement. Such information should enable both conventional breeding- and biotechnology-driven improvements, whilst, at the same time, reveal fundamental knowledge about tree development and the mechanisms by which they have repeatedly evolved. Here, we break down some of the major developmental components of tree architecture and summarize the current knowledge for each. This is followed by descriptions of several common mutant New Phytologist (2015) 206: 541–556 www.newphytologist.com

tree forms and what has been learned from genetic studies of these traits.

II. Components of tree architecture 1. Architectural units The most fundamental unit of plant architecture is the phytomer. Phytomers comprise an internode plus a node with one or more leaves that contain lateral vegetative and/or floral meristems, known as buds (Fig. 1a) (McSteen & Leyser, 2005). One or more phytomers make up larger architectural units that are repeated throughout a plant in a process called reiteration (Tomlinson, 1983; Barthelemy & Caraglio, 2007). Their arrangement specifies basic plant topography. Reiteration also occurs in response to environmental stimuli. For example, as temperate tree species transition out of winter dormancy, some of the lateral vegetative buds will initiate growth and reproduce the main stem structure situated on a more horizontal axis. Branch reorientation caused by bending or leaning, or by shoot damage or decapitation, can also lead to reiteration (Tomlinson, 1983; Barthelemy & Caraglio, 2007). The differential growth of numerous branches that reiterate the main stem give trees their overall shape and canopy structure. In connection with phytomer structure and arrangement, the location of floral buds and vegetative buds also shapes tree appearance (Tomlinson, 1983; Lauri et al., 1995, 2010; Wilson, 2000; Barthelemy & Caraglio, 2007). When flowers are pollinated and produce fruit, the fruit weight often leads to branch bending. This reorientation of the branch can result in a gravitropic response which will cause the shoot tip to grow upwards. At the same time, the tension force caused by the fruit weight promotes structural (a)

(b)

(c)

Fig. 1 A plum sapling illustrating a phytomer (a) and the concepts of apical dominance and apical control (b and c). The primary shoot in (b) was decapitated, releasing apical dominance over an inferior below and promoting shoot growth. This new shoot is not influenced by apical control and grows vertically, becoming the new leader. (c) Two branches grow out of a decapitated shoot. The upper shoot grows vertically. The lower shoot is under the influence of apical control and grows at an angle. *, Vegetative buds that remain dormant because of the influence of apical dominance from the growing shoot above them. No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist changes in the branch (the development of reaction wood) in order to support and/or bend the branch upwards (Brown, 1971a; Wilson & Archer, 1977). Over time, repeated seasons of growth, fruit set and reaction wood formation significantly shape overall tree architecture. This is well illustrated in apple trees with the type IV architecture. Type IV apples have long lateral shoots that weep or grow downwards at their shoot tips. These trees repeatedly set fruit on the ends of their branches, the weight of which enhances their weeping-like appearance (Lespinasse, 1977, 1992; Segura et al., 2007; Lauri et al., 2008). Likewise, alternate bearing, a condition in which trees display high fruiting in one year followed by low fruiting in the following year, can similarly impact architecture (Monselise & Goldschmidt, 1982; Lauri et al., 1995, 2014). Vegetative buds, unlike floral buds, do not initiate growth all at once in the springtime. Depending on environmental conditions, they can either initiate growth and produce a lateral branch or remain dormant for an indefinite period of time. Vegetative growth, when it occurs, can be sylleptic, meaning that growth occurs in the same season as bud formation, or proleptic, where the bud undergoes a period of dormancy (Tomlinson, 1983; Wilson, 2000). There is substantial knowledge concerning sylleptic and proleptic growth, as well as bud dormancy, and their connections to genetic, epigenetic and hormonal pathways. These concepts have been described elsewhere and will not be emphasized here (Cook et al., 1999; Segura et al., 2007; Cooke et al., 2012; Van der Schoot et al., 2014). After vegetative buds break and begin to grow into new shoots, they exhibit either upward (orthotropic) or outward (plagiotropic) growth. Orthotropic branches are upright or vertical and exhibit radial symmetry, whereas plagiotropic branches grow horizontally and have dorsal–ventral symmetry (Sterck, 2005). 2. Apical dominance and apical control Apical dominance and apical control both involve the influence of a primary shoot apex, or leader, on the growth of subordinate plant meristems and branches (Cline, 1997; Wilson, 2000; Dun et al., 2006). Apical dominance, which impacts axillary bud outgrowth, has been studied in numerous plant species (Cline, 1997). By contrast, relatively little is known about apical control, which has been primarily associated with trees and describes the role played by the primary shoot apex on the entire branch complex of a plant (Wilson, 2000). Both of these phenomena have crucial roles in shaping the architecture of trees. Apical dominance is the repression of lateral vegetative bud outgrowth by the shoot apical meristem, enabling plant resources to primarily be used for elongation of the leader (Fig. 1) (Cline, 1997; Sterck, 2005). This also applies to the ability of lateral branch apical meristems to inhibit growth of their own subordinate axillary buds. By repressing bud outgrowth, apical dominance is one factor responsible for proleptic shoot growth (Wilson, 2000; Turnbull, 2005). Subordinate buds repressed by apical dominance will remain dormant and will not break until they are released. Bud release can be triggered by external factors, such as plant damage, branch reorientation or changes in light. Branch bending can release repressed vegetative buds when the apical shoot becomes No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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reoriented beneath its subordinate buds. Meristem decapitation will lead to a release of apical dominance on buds closest to the point of apex removal, whereas lower buds will remain dormant (Fig. 1b, c) (Cline, 2000). Thus, the outgrowth potential of each bud varies with respect to its position on the stem (Turnbull, 2005). Another condition affecting apical dominance is light. High light triggers the release of apical dominance to promote lateral shoot growth – an adaptation that probably developed to maximize photosynthetic capacity. By contrast, trees under low light conditions often maintain strong apical dominance to facilitate upward growth of the leader towards light (Sterck, 2005). Over 80 yr of research have attributed apical dominance to a basipetal auxin concentration gradient that results from the rootward movement of the plant hormone auxin (Wickson & Thimann, 1958; Stafstrom & Sussex, 1992; Beveridge et al., 1994; Wang et al., 1994; Cline, 1997, 2000; Sterck, 2005; Turnbull, 2005). Experiments in herbaceous plants, as well as more recent ones in trees (Wang et al., 1994; Cline, 2000; Turnbull, 2005), have shown that large amounts of auxin in the apex, where it is synthesized, inhibit the growth of lateral buds on the same stem. A reduction of auxin by decapitation or application of transport inhibitors triggers the release of apical dominance and promotes lateral bud outgrowth (Hall & Hillman, 1975; Stafstrom & Sussex, 1992; Turnbull, 2005). Classic experiments by Thimann & Skoog (1933) utilized auxin-infused agar blocks to successfully replace the apical meristem and inhibit bud release in bean and oat plants. Cline (2000) found the same result when applying exogenous auxin to decapitated ash trees. Repression of bud growth is, at least in part, caused by the ability of auxin to repress cytokinin (CK) synthesis at the nodes and its transport into the dormant buds, where it can activate cell cycle genes (Sachs & Thimann, 1967; Pillay & Railton, 1983; Cline, 1997; Tanaka et al., 2006; Ferguson & Beveridge, 2009). Application of CK to dormant lateral buds eliminates the apical dominance acting on these buds and initiates growth. Once growth proceeds, the developing lateral shoot tips produce auxin, which then initiates vasculature development as it travels towards the main shoot, and inhibits the growth of its own newly developed axillary buds (Cline, 1997; McSteen & Leyser, 2005; Sterck, 2005). The hormone strigolactone (SL) is believed to act as a second messenger that works with auxin to maintain apical dominance (Ferguson & Beveridge, 2009; Cheng et al., 2013). Arabidopsis and pea with interrupted SL biosynthesis or signaling have a high degree of bud break, giving rise to plants with a high degree of branching (Gomez-Roldan et al., 2008; Cheng et al., 2013). The role of SL has not been well studied in trees, but it seems likely that it also plays a role in maintaining apical dominance. Recent work is now challenging the long-standing dogma regarding the role of auxin in mediating apical dominance. A study in pea plants by Mason et al. (2014) has suggested that the sugar supply and not auxin is the key signal regulating apical dominance. The authors found that sucrose levels rise in lateral buds following decapitation, and the application of sucrose alone to lateral buds could stimulate bud break. They offered a model whereby decapitation leads to the increased availability of sugar supplies to lateral buds, triggering their release from dormancy (once a certain threshold has been crossed), whereas auxin functions to prioritize New Phytologist (2015) 206: 541–556 www.newphytologist.com

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subsequent stages of bud outgrowth. Further experimentation in both model plants and trees is needed to confirm which factors are responsible for apical dominance, which are simply correlative, and whether the same mechanisms are responsible in different plants and trees. A unique feature of apical dominance in trees is that, in the absence of decapitation, it only affects the lateral buds on the current year of growth (Brown et al., 1967). The slow rate of rootward auxin movement through a tree prevents the auxin produced in the main apex from influencing new buds on lateral branches further down the main stem (Sundberg & Uggla, 1998; Cline, 2000). Current year lateral buds on an actively growing leader are thought to be inhibited by auxin from their apical meristem, whereas current year buds formed on lateral branches are inhibited only by auxin from the same axillary shoot meristem. It is important to specify that, although apical dominance is spatially limited in trees, the apex still exerts control over the growth and development of the entire tree. This phenomenon, known as apical control, influences several aspects of growth, including branch angle, branch length and stem diameter (Wilson, 2000; Sterck, 2005). The angle of a primary branch relative to a main stem is one of the key architectural features regulated by apical control (Wilson & Archer, 1981). Lateral branches near the base of the tree are typically oriented outwards, growing horizontally, whereas those closer to the apex grow at an upward angle. When the main shoot is decapitated, a lateral branch or branches (initiated from a dormant bud or already present) will bend and grow vertically to take the place of the removed leader (Fig. 1b,c). Apical control also regulates branch diameter, a phenomenon described by Leonardo da Vinci in the 15th century (Wilson, 2000; Minamino & Tateno, 2014). In his rules for tree growth, da Vinci pointed out that the diameter of all the branches of a tree, when removed and bundled together, equals the diameter of the main trunk, regardless of the age or type of the tree. The relative accuracy of this phenomenon has been illustrated in several studies using both plant measurements and computer modeling (Sterck, 2005; Sone et al., 2009; Minamino & Tateno, 2014). Mechanisms behind apical control are poorly understood, but the bending of lateral branches in decapitated trees suggests that auxin has a role in this phenomenon (Wilson, 1973, 2000; Wilson & Archer, 1981; Cline, 1997). Carbon sink strength between branches and the trunk may also play a role in the regulation of branch growth and positioning through apical control (Wilson & Archer, 1981; Sterck, 2005). Girdling (cutting a ring around a trunk) above or below a branch prevents phloem transport and can release apical control, as indicated by an increase in branch diameter (Wilson & Archer, 1981, 1981). Ratios or localizations of CK, gibberellic acid (GA) and ethylene, as well as hydraulics and nutrient transport, may also be involved in growth regulation directed by apical control (Blake et al., 1980; Tomlinson, 1983; Wilson, 2000), but, at this time, it is not clear which are causative signals and which are downstream responses. Overall, the combined action and relative degree of both apical dominance and apical control influence tree crown shape. This control is genetically predetermined for each species, although New Phytologist (2015) 206: 541–556 www.newphytologist.com

environmental conditions can temporarily alter the degree of influence. Trees with innately strong apical dominance and strong apical control, such as conifers, tend to have oblong or pyramidal crown shapes (Brown, 1971b; Cook et al., 1999). Their main trunk grows tallest, the lateral branches grow more outwards than they do upwards, and the branches closest to the apex are shorter in length. This type of growth is called excurrent growth. Trees with no prevailing leader as a result of weak apical dominance tend to have branches of different sizes at different positions and angles, resulting in round or oval crowns. This type of growth is described as decurrent growth, and examples include sweet gum and tulip poplar trees (Brown, 1971b). Many trees exhibit varying degrees of apical control and apical dominance, and do not fall into either of these extreme categories. 3. Branch angles and orientation Branch angles influence many aspects of tree biology, including light interception and competition with neighboring trees. The angle of a lateral branch from its originating shoot has three components. The first is the initial crotch angle, or the angle of the shoot at the point of connection to the branch. This angle is established at shoot initiation. As branches elongate, a second growth trajectory is established. In trees, this angle, formed between the main stem and the direction of branch growth, has been termed both the equilibrium angle (Wilson, 2000) and the angle of inclination (Brown, 1971b). In Arabidopsis, others have named it the gravitational set point angle, as it is dependent on the perception of gravity by the plant (Digby & Firn, 1995; Roychoudhry et al., 2013). Interestingly, when external conditions alter the equilibrium angle, the shoot always returns to its initial angle of growth through a combination of bending and new growth (Wilson, 2000; Roychoudhry et al., 2013). It has also been suggested that the nonvertical growth behavior of axillary shoots is caused by an unknown anti-gravitational force (Roychoudhry et al., 2013). The third component of branch angle is the geotropic angle. This angle occurs at the very tip of actively growing lateral branches and may be more upward, or sharper, than the other angles because of the lack of secondary growth in this region (Brown, 1971b). Conifers with high apical control and primarily plagiotropic growth have wide branch angles and an outward orientation of branch growth. However, branch growth orientation does not always correspond closely to the initial crotch angle. Branches of trees with the weeping growth habit compared to standard forms (Fig. 2a,b) have narrow and upward branch angles, yet, at some point during development, their branches turn downward. All subsequent growth is in a rootward direction, resulting in branches with a downward orientation. In Arabidopsis and pea plants, branch angle specification has primarily been attributed to gravitropic responses. However, trees, which have higher orders of branching as well as extensive secondary growth, are more architecturally and developmentally complex. The understanding of branch development and orientation in herbaceous species may not be sufficient to describe all aspects of tree architecture. The crotch angles and equilibrium angles in trees exist relative to the shoot from which they initiate, are No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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(d)

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(e)

(f)

(h)

(g)

Fig. 2 Examples of distinct tree architectures with the genotypes indicated. (a) Standard peach growth habit. (b) Weeping peach (pl/ pl ). (c) Pillar peach (br/br). (d) Columnar apple (co/co or co/+). (e) Pillar trees providing attractive low-maintenance beautification of a city street. (f) Upright peach (br/+). (g) Archer tree (pl/pl; br/+). (h) Brachytic dwarf (dw/dw) beginning to leaf out. (i) A72 dwarf peach (n/n). Inset shows forked branching. (j) A72 semi-dwarf tree (n/+) next to a sibling with standard architecture. (k) Compact peach (ct/ct or ct/+).

(j)

consistent throughout a plant and are genetically determined (Fisher & Honda, 1979; Tomlinson, 1983). Although a secondary or tertiary branch may grow outwards or downwards, it will have the same equilibrium angle as a first-order branch. This has been described as the rule of branching and has been observed in many plant species. These genetically determined branching angles are not relative to the gravity vector or direction of the main shoot. Thus, tree branch angles and branch orientation may be more reliant on hormone gradients or another form of communication between the lateral meristems and their parent branch than on gravitropic sensing. 4. Reaction wood The ability of trees to develop reaction wood is an important component that shapes their overall branch architecture. Reaction No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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(i)

(k)

wood is a specialized type of wood that forms in response to mechanical stress imposed by the weight of tree limbs as they increase in size. It can also result from other stresses, including the weight of snow or heavy fruit set, as well as high winds. Reaction wood may also develop to support tree trunks after incidents that cause them to lean. There are two types of reaction wood, each identifiable by visualizing the cell structure of cross-sections under a microscope. The first, compression wood, is present in gymnosperms and forms on the lower side of the branches in the region of mechanical stress. Compression wood prevents branches from sagging downwards by the expansion of cells along the lower side of the stem, coupled with increased lignin content in the secondary cell walls and thickening of the tracheid walls (Wilson & Archer, 1977; Guerriero et al., 2014). Tension wood, the second type of reaction wood, is unique to angiosperms. Tension wood forms on the upper side of branches, New Phytologist (2015) 206: 541–556 www.newphytologist.com

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is low in lignin content, high in cellulose and acts to pull branches upwards through cellular contraction (Wilson, 2000; Guerriero et al., 2014). Tension wood is discernible by its small dense cells and cell walls with gelatinous fibers (Wilson & Archer, 1977; Guerriero et al., 2014). Many hardwoods develop regions of tension wood to support their branches under normal conditions. However, Wilson & Archer (1983) showed that Prunus serotina and Fraxinus americana branches lacked tension wood until decapitated. On decapitation, the branches developed tension wood and bent upwards, allowing them to replace the removed leader – suggesting that tension wood formation is, at least in part, regulated by apical control. The formation of reaction wood has been associated with auxin redistribution. Tension wood forms in regions with low auxin, and is inhibited by auxin application (Kozlowski, 1971; Timell, 1986; Little & Savidge, 1987; Sundberg et al., 1994). However, the role of auxin in this process remains controversial, as Hellgren et al. (2004) and Moyle et al. (2002) did not observe an auxin gradient across stems bent to stimulate tension wood formation. Yet, it should be noted that Moyle et al. found the differential expression of auxin response genes in the upper cambial region. Further dissection of these aspects of secondary growth is not only important for the optimization of tree architecture, but is of particular importance to timber industries as they significantly affect wood qualities. 5. Stem diameter and branch size The thickness of tree branches contributes to both their tensile strength and their ability to transport water and nutrients. This architectural feature has therefore been considered as a key factor shaping tree structure. Although very little is known about the molecular or genetic mechanisms involved, the physiological effects have been well documented. Various hypotheses have been proposed to explain branch diameters within a tree and how branch diameter, tensile strength and hydraulic conductance modulate growth. A number of mathematical models have been derived to predict tree form, including the pipe model, power law scaling and fractal dimensioning (reviewed by Dahle & Grabosky, 2009). The pipe model theory, proposed by Shinozaki et al. (1964a,b), has been successfully used (albeit to a limited extent) to model tree growth dynamics in forest ecosystems. The pipe model considers each reiterated segment of a tree as a distinct unit, capable of supporting a certain amount of photosynthetic tissue. According to the model, the total leaf mass supported by a branch can be predicted by the stem diameter. Thus, tree shape is strongly influenced by the rate and patterning of branch development, which serves to provide energy and resources to the entire system. Tree growth simulators, such as L-PEACH, have built upon these principles and have been designed to predict overall development based on source–sink relationships involving carbon and nutrient allocation in response to water deficit and fruit thinning (Allen et al., 2005). The biological features that underpin these aspects of tree branch function remain poorly understood at the molecular and genetic levels, although they undoubtedly involve a range of

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features related to xylem and phloem function coupled with wood chemistry.

III. Tree architecture categorizations Using simple observations, 23 architectural models have been generated to describe the genetically predetermined growth habits of trees in unstressed environments (Halle et al., 1978; Tomlinson, 1978). Each model is named after a scientist who studied one of the representative trees. These architectures are universal descriptions of tree growth throughout the plant kingdom and are not limited to one species or genus. Different architectural models can be found in trees of the same species (Tomlinson, 1978). Although most of the 23 models describe trees from tropical regions, where there is a high degree of diversity, several accurately describe temperate conifers and hardwood trees. For example, Rauh’s model describes trees with a monopodial trunk, whorled orthotropic branches that are identical to the trunk and lateral flowering (in angiosperms). This model applies to pine, oak, maple and peach trees, among others. Architectures specific to apple trees have also been categorized (Lespinasse, 1977, 1980, 1992; Lauri et al., 1995) into four classes, I–IV, based on growth and flowering. Type I apples have a columnar form with minimal secondary branching and many spurs (short terminal branches that produce flowers and fruit, emerging from their prominent main trunk). Type IV trees have vigorous growth, fruit set at the top of the tree and tips of branches, higher orders of branching and (as mentioned earlier) a weeping appearance at their branch tips. The other two types have intermediate growth styles; type II bears fruit from spurs on its few upright branches and type III has medium and long branches and few spurs. In addition to detailed growth categorizations of common tree architectures, several non-standard tree growth habits have been described. Trees with these abnormal forms provide a starting point for understanding the complex developmental processes that determine tree architecture. Just as the phenotypes of plants with gene mutations help to deduce the normal roles of these genes in wild-type plants, the study of the molecular mechanisms behind non-standard tree architectures can help to elucidate how tree shape is developmentally controlled. Previously described non-standard tree architectures include columnar or pillar (Fig. 2c–e), weeping (Fig. 2b), dwarf and semi-dwarf (Fig. 2h–j), and compact or highly branched (Fig. 2k). These atypical forms have been at least partially characterized at the molecular level. We describe below the known biology behind these growth habits. The genetic studies of these tree forms have largely been limited to several model tree species, which include peach (Prunus persica), apple (Malus 9 domestica Borkh), birch (Betula sp.) and poplar (Populus sp.). These species all have sequenced genomes (Table 1), as well as some examples of monoallelic traits for non-standard architectures. As of the date of this review, at least 20 tree genomes have been published (Table 1). The availability of these genomes is aiding in the identification of the underlying genes and pathways that control key aspects of tree architecture.

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Table 1 Published tree genomes Common name

Scientific name

Reference

African oil palm Apple Banana Black cottonwood Cacao Date palm

Elaeis guineensis

Singh et al. (2013)

Malus 9 domestica Borkh. Musa acuminata Populus tricocarpa

Velasco et al. (2010) D’Hont et al. (2012) Tuskan et al. (2006)

Theobroma cacao Phoenix dactylifera L. Betula nana Prunus mume Pinus taeda Morus notabilis Picea abies Carica papaya Linnaeus Prunus persica Pyrus bretschneideri Rehd Hecea brasiliensis Betula pendula Elaeis oleifera

Argout et al. (2011) Al-Mssallem et al. (2013) Wang et al. (2013) Zhang Q et al. (2012) Zimin et al. (2014) He et al. (2013) Nystedt et al. (2013) Ming et al. (2008) Verde et al. (2013) Wu et al. (2013) Rahman et al. (2013) birchgenome.org Singh et al. (2013)

Citrus sinensis Picea glauca Eucalyptus grandis

Xu et al. (2013) Birol et al. (2013) Myburg et al. (2014)

Dwarf birch Japanese apricot Loblolly pine Mulberry Norway spruce Papaya Peach Pear Rubber tree Silver birch South American oil palm Sweet orange White spruce Eucalyptus

IV. The molecular basis for non-standard tree architectures 1. Columnar/pillar tree architectures Trees having a narrow canopy and overall vertical growth habit can be found in a variety of gymnosperms and angiosperms. This growth type is commonly referred to as fastigiated in landscape nurseries. Fastigiated trees have shorter branches, narrow crotch angles, exhibit strong apical dominance and have strong agravitropic phenotypes (Fig. 2c). Their slender profile, which minimizes the need for pruning, is one reason for their common use in urban landscapes (Fig. 2e), as well as by home growers. Breeders have also recognized the potential value of fastigiated fruit trees, which can be planted in higher density and have the potential to give higher yields than standard trees (Scorza et al., 1999). This growth habit has been described in the scientific literature as either pillar (e.g. pillar peach) or columnar (e.g. columnar apple). Although similar in profile when in full foliage, the two growth habits have some key distinctions (Fig. 2c,d) and different genetic causes. By contrast with the pillar peach architecture, the columnar apple, a type I class apple, has very few lateral branches (Fig. 2d), suggesting that it has a stronger apical dominance than standard trees. The branches that are present, however, are similar to those of the peach pillar in that they have narrow crotch angles and are shorter in length than those of standard trees (Tworkoski et al., 2006; Petersen & Krost, 2013). 2. Pillar peach The peach pillar phenotype segregates as a single semi-dominant gene, originally named broomy (br) for its ‘broomy’ appearance No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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(Yamazaki et al., 1987). Although br/br trees have an entirely columnar or pillar appearance, heterozygous individuals show a more spreading ‘upright’ phenotype (Fig. 2f) (Scorza et al., 1989, 2002; Tworkoski & Scorza, 2001). Physiological studies have shown that pillar peach trees display a range of physical alterations, including shorter lateral shoots (a result of shorter internodes), smaller stem diameter, decreased sylleptic branching and narrow crotch angles (Tworkoski & Scorza, 2001; Tworkoski et al., 2006). In addition, auxin-to-CK ratios were found to be higher throughout the canopy of pillar trees. The observed pleiotropic effects suggest that the underlying gene regulates a general feature of plant growth and development. The br locus was mapped by several groups to peach genome linkage group 2 using microsatellite markers (Sosinski et al., 2000; Dirlewanger et al., 2004; Sajer et al., 2012). More recently, the causative allele was identified in the same region using a novel method involving next-generation sequencing (Dardick et al., 2013). The disrupted gene, ppa010082, was not expressed in pillar trees and showed reduced expression in upright heterozygous trees (Dardick et al., 2013). Ppa010082 was found to be an ortholog of the rice gene TILLER ANGLE CONTROL 1 (TAC1) (Yu et al., 2007). In rice and maize, mutations in the 30 UTR of TAC1 were associated with reduced gene expression and an upright tiller growth habit (Yu et al., 2007; Ku et al., 2011). These alleles have been previously bred into cultivated rice and maize varieties to enable high-density planting. Two distinct null alleles in peach were found in different genetic sources of the pillar trait, one originating from Japan and the other from Italy. Likewise, a T-DNA disruption in the Arabidopsis ortholog AtTAC1 (At2g46640) resulted in plants with narrow branch angles (Dardick et al., 2013). Over-expression of the AtTAC1 gene in Arabidopsis was only able to partially complement the mutant phenotype, indicating that a certain optimal level of expression is required for normal branch orientation. Taken together, these findings suggest that expression levels of the TAC1 gene are important for correct branch orientation. More specifically, precise amounts of TAC1 expression are important for the promotion of wide branch angles, as the null mutants have very narrow branch angles. The mechanism by which TAC1 affects branch or tiller growth angles is currently unknown, but the finding that TAC1 functions in grasses, herbaceous plants and trees suggests that the developmental pathways controlling lateral shoot angle are perhaps universal. BLAST searches showed that TAC1 genes are present as a single copy or as a small family in a broad range of plant species (Dardick et al., 2013). Interestingly, TAC1 genes were found to form a larger gene family (named IGT for a highly conserved motif) that includes another branch angle control gene called LAZY1 (Fig. 3) (Dardick et al., 2013). Silencing of LAZY1 produces the opposite phenotype to tac1 and leads to horizontal growth of Arabidopsis inflorescence lateral shoots and rice tillers, as well as weak agravitropic responses (Li et al., 2007; Yoshihara & Iino, 2007; Yoshihara et al., 2013). In maize, in which LAZY1 was found to be light regulated, mutations also caused aberrant fruit development and increased polar auxin transport (Dong et al., 2013; Howard et al., 2014). TAC1 and LAZY1 proteins share four New Phytologist (2015) 206: 541–556 www.newphytologist.com

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conserved domains, whereas most LAZY1 members have a unique C-terminal domain comprising an ethylene-responsive elementbinding factor-associated amphiphilic repression (EAR) motif (LxLxL). EAR motifs are known to repress auxin response genes and may provide a mechanism of action for LAZY1 (Tiwari et al., 2004; Dong et al., 2013; Yoshihara et al., 2013). The finding by Tworkoski et al. (2006) that pillar peach trees have higher levels of auxin in lateral shoots suggests that, in contrast with LAZY1, wildtype TAC1 may promote polar auxin transport. Uga et al. (2013) recently identified a gene called Deep Rooting1 (DRO1) which, although not initially reported, is also an IGT family member (Fig. 3). Expression of DRO1 was shown to be limited to root tissues and was negatively regulated by auxin. DRO1 controls the elongation of root tip cells, leading to asymmetric root growth and downward bending in response to gravity. Downwardoriented root growth was associated with higher DRO1 levels (Uga et al., 2013). Thus, DRO1 action in roots represents the mirror image of LAZY1 action in shoots. DRO1 orthologs are also found in many different plant species and represent a distinct clade from TAC1 and LAZY1. DRO1 proteins share the conserved C-terminal EAR motif that is also found in LAZY1. Phylogenetic analysis indicates that LAZY1 and DRO1 are more ancient than TAC1, as the IGT genes found in mosses and lycophytes are more similar to LAZY1/DRO1 and their proteins also contain the EAR motif (Fig. 3). TAC1 is only found in higher plants and appears to have arisen concurrently with the development of axillary shoots (Dardick et al., 2013). Collectively, these data suggest that TAC1 may have evolved from a LAZY1 or DRO1 ancestor, and the lack of

a C-terminal EAR motif may suggest that it functions as a repressor of LAZY1 and/or DRO1. Although both LAZY1 and DRO1 proteins localize to the cell membrane, cellular localization studies for TAC1 have not yet been reported (Uga et al., 2013; Yoshihara et al., 2013). LAZY1 was also found in the nucleus, but nuclear exclusion through mutation of the nuclear localization signal did not impact gene function in Arabidopsis (Yoshihara et al., 2013). Further study of IGT genes will undoubtedly shed light on the mechanisms governing lateral branch orientation in trees and the role of auxin in this process. 3. Columnar apple All commercial columnar apple trees, known as Wijcik, originated from vegetative propagation of a McIntosh sport discovered in 1961 that had a somatic mutation (Lapins, 1969a; Petersen & Krost, 2013). As described above, columnar apples have short branches with narrow branch angles and numerous spurs (Fig. 2d). In addition, Wijcik trees have short, thickened internodes leading to a reduced overall tree height (Lapins, 1969b; Petersen & Krost, 2013), a trait that is agriculturally beneficial to growers. Wijcik trees require significantly less pruning, produce fruit close to the primary stem and sometimes exhibit more frequent alternate bearing  ıcek, 2012). It should be noted that the (Dokoupil & Rezn columnar architecture was initially described as having a compact growth habit (Lapins, 1969a). The term compact is now more commonly used to describe trees with either excessive branching or a semi-dwarf stature (discussed in section IV.6).

Fig. 3 Unweighted pair group method with arithmetic mean (UPGMA) topological tree showing the relationship between IGT gene family members TILLER ANGLE CONTROL 1 (TAC1), LAZY1 and Deep Rooting 1 (DRO1) in several monocot and dicot species, as well as moss and spike moss. Species were selected based on the availability of the whole genome sequence. The multiple alignment was performed on protein sequences using MUSCLE (Edgar, 2004), followed by manual refinement. Bootstrap values are shown at each node. Brown lines, clustering of DRO1 genes; green lines, clustering of LAZY1 genes; orange lines, clustering of TAC1 genes; blue lines, the outgroup of the more ancient LAZY1-like genes in Physcomitrella (moss) and Selaginella (spikemoss). Both DRO1 and LAZY1 genes (including the moss and spike moss genes) contain a C-terminal EAR motif. New Phytologist (2015) 206: 541–556 www.newphytologist.com

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New Phytologist Numerous researchers have attempted to map this single dominant trait (co) to design molecular markers for breeding. Despite several extensive genetic mapping projects and transcriptome studies (Bai et al., 2012; Krost et al., 2012, 2013; Zhang Y et al., 2012; Otto et al., 2014), the precise nature of the co allele remains puzzling. To date, co has been fine mapped to a c. 196-kb region with 26 predicted genes on linkage group 10 of the golden delicious apple genome (Moriya et al., 2012). Bai et al. (2012) proposed that Co is one of the three LATERAL ORGAN BOUNDARIES DOMAIN (LBD) genes in this region. LBD genes are plant-specific transcription factors with known roles in lateral organ development, root initiation, embryo and leaf development, and secondary growth (Majer & Hochholdinger, 2010; Yordanov et al., 2010; Coudert et al., 2013). More recently, Wolters et al. (2013) provided evidence that the Wijcik growth habit is caused by insertion of a 1956-bp noncoding DNA element within an intergenic region upstream of an Fe(II) oxygenase gene they named MdCO31. This gene is located upstream of the insertion, but still within the 196-kb mapped region of chromosome 10 (Moriya et al., 2012; Wolters et al., 2013). This same DNA insertion in the Co locus was identified as a Ty3/Gypsy retrotransposon by Otto et al. (2014). Both groups found no other nucleotide changes within the mapped co region, suggesting that this retroelement is somehow responsible for the phenotype. After comparing expression levels of the genes in the chromosome 10 region by quantitative reverse transcriptionpolymerase chain reaction (qRT-PCR), Wolters et al. (2013) suggested that the phenotype results from the upregulation of MdCO31 in vegetative buds. They showed that Arabidopsis overexpressing MdCO31 was compact in structure and had short floral internodes. Fe(II) oxygenases are involved in the biosynthesis of ethylene, flavonoids, GA and defense responses, and could potentially explain the co phenotype. By contrast, using RNAseq, Otto et al. (2014) found an association between the retroelement and the differential expression of a large number of genes. You et al. (2014) suggested that the columnar apple phenotype is connected to gene regulation by microRNAs (miRNAs). Transgenic apples trees that over-expressed the apple Double Stranded RNA Binding Protein 1 (MdDRB1) produced trees with a phenotype similar to Wijcik (You et al., 2014). MdDRB1 is involved in miRNA processing and maturation. You et al. hypothesized that MdDRB1 regulates an miRNA that controls LBD genes, such as those identified by Bai et al. (2012). An intriguing possibility is that the gypsy retroelement identified by Wolters et al. (2013) and Otto et al. (2014) alters gene expression through differential miRNA expression and/or function. A number of transcriptomic studies, using both microarrays and RNAseq, have compared Wijcik and McIntosh gene expression (Krost et al., 2012; Zhang Y et al., 2012; Otto et al., 2014). Collectively, they showed that Wijcik, compared with the standard McIntosh control, shows differential expression of genes involved in IAA, GA and brassinosteroid (BR) homeostasis. Differential expression of cell membrane and cell wall genes was also reported. These findings are consistent with the phenotype, in that IAA, GA and BR regulate growth through cell and internode elongation and cell membrane/cell wall composition. No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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In summary, the mechanism responsible for the Wijcik columnar apple phenotype appears to be complex. Further studies are needed to uncover how insertion of the identified retrotransposon alters gene expression to give rise to the columnar phenotype. What is clear, however, is that the apple columnar and peach pillar traits are not caused by mutations within the same genes. Whether they are a result of impairments in the same core pathway or mechanism remains to be determined. 4. Molecular mechanisms associated with weeping architecture The weeping growth habit is easily recognizable by its pendulous downward-growing branches (Fig. 2b). Over 500 weeping tree cultivars have been described, including commonly grown weeping willow and weeping Japanese cherry trees (Govaerts et al., 2011). Weeping shoots initially grow upwards but, at some point in their development, for unknown reasons, their tips bend downwards and continue growth in this direction. The downward bending of the branch apex releases one or more subordinate lateral buds from apical dominance, promoting new shoot development along the highest point in the branch (Brown, 1971b). The new branches then repeat this bending process. Interest in this growth habit stems from its use in ornamental trees, as well as in novel training methods for orchard production (Werner, 1985; Moore et al., 1993; Scorza et al., 1999; Fideghelli et al., 2003; Werner & Chaparro, 2005). The type IV apple has also been described as weeping (Sampson & Cameron, 1965; Lespinasse, 1977, 1980). In contrast with the architecture of weeping willow, cherry and peach (among many others), the branches of type IV apple trees grow more outwards and upwards, not necessarily pendulous. Only the ends of their branches bend downwards as a consequence of fruit weight (Lespinasse, 1980). We will not discuss these weeping-like architectures further and instead focus on the more common pendulous weeping trait. The pendulous weeping phenotype in peach, described by Monet et al. (1988), Bassi et al. (1994) and Bassi & Rizzo (2000), segregates as a monogenic recessive trait. The representative allele has been designated as both pleurer (pl ) and weep (we). Initially described as recessive, more recent observations of a subtle heterozygous phenotype suggest incomplete dominance (Bassi & Rizzo, 2000). The pl allele has been placed on two separate linkage maps. Dirlewanger & Bodo (1994) mapped peach pl to their linkage group 2 (not to be confused with LG2 of the peach genome assembly from Verde et al., 2013) between markers p14-1500 and p14-1150. Chaparro et al. (1994) associated pl with the allele for white flower (w) in a region linked with the Ps2 molecular marker. The trait has not yet been fine mapped or associated with any region or allele in the 2013 draft peach genome (Verde et al., 2013). The pl phenotype may be attributed to either aberrant GA signaling and/or alterations in wood composition. Weeping branch internodes are longer than those in standard trees (Fideghelli et al., 2003), suggesting a possible upregulation in GA biosynthesis or response. In addition, as the shoots bend downwards as growth progresses, but not from the start, the weeping growth habit has also been attributed to a lack of mechanical rigidity from improper New Phytologist (2015) 206: 541–556 www.newphytologist.com

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timing between shoot elongation and the formation of lignified secondary xylem (Brown, 1971b; Nakamura et al., 1994). Testing these two hypotheses, Baba et al. (1995) applied GA3 to Japanese weeping cherry branches. Application of the hormone led to an increase in weeping shoot diameter, the production of tension wood regions similar to those in the standard cherry branch, and an upward growth orientation. Nakamura et al. (1995) later produced the same result when applying GA to weeping peach branches. Yoshida et al. (1999) repeated and furthered this study by measuring growth stress in GA-treated and untreated weeping cherry branches. The GA-treated branches developed upright growth and had more tensile stress that caused tension wood formation at the start of the secondary wood growth phase. The untreated weeping branches also developed tension wood, but not until later in the growth period (Yoshida et al., 1999), suggesting that there is a timing requirement for the formation of tension wood in order to suppress downward growth. Later, Sugano et al. (2004) found higher levels of GA3 oxidase, an enzyme that produces bioactive GA, and a higher level of GA in the elongation zones of weeping shoots compared with upright Japanese flowering cherry (Prunus spachiana). Taken together, these results suggest that correct temporal regulation of GA-induced shoot growth triggers early secondary growth development (reaction wood). Perhaps if the GA levels are not active early enough, the weeping habit may arise. The association between wood composition and weeping architecture was also illustrated in poplar with the suppressed expression of cellulose synthase genes (Joshi et al., 2011). Cellulose in the cell wall acts as a scaffold for xylans and lignin during secondary wall formation and is essential for cell wall strength. Poplar with reduced cellulose synthase showed a significant decrease in cellulose content in secondary cell walls, coupled with an increase in lignin and non-cellulosic polysaccharides (Joshi et al., 2011). As a result, these trees produced a weeping growth habit with an appearance similar to weeping peach and cherry. An altered gravitropic response may also be responsible for the weeping phenotype, at least in some species. The main shoot of a gravitropic mutant of Japanese morning glory (Ipomea nil ) has a weeping architecture similar to weeping peach. Two causative weeping alleles were identified in morning glory (we1 and we2) (Kitazawa et al., 2005, 2008). Both genes were associated with agravitropic phenotypes. WE1 is an ortholog of Arabidopsis SCARECROW (SCR), and WE2 is an ortholog of Arabidopsis Short-Root (SHR). SCR and SHR are GRAS family transcription factors that are essential for the development of the endodermis and normal gravitropic responses (Fukaki et al., 1998; Tasaka et al., 1999). Based on current analysis of various weeping plant species, a number of different genetic factors may be responsible for this growth habit. Abnormalities in GA content, timing of reaction wood formation and altered gravitropism may underlie various weeping traits, but it is not clear which of these phenomena are causes or consequences of the non-standard weeping allele. Other aspects of developmental regulation that have yet to be discovered may also be needed for trees to maintain upright or vertical growth. Although the weeping phenotypes are very similar among the New Phytologist (2015) 206: 541–556 www.newphytologist.com

species mentioned here, it is possible that the alleles in each species do not code for orthologous genes. Interestingly, an unexpected genetic interaction was found between pl and br, the peach pillar allele. The pillar phenotype was shown to be epistatic to the weeping phenotype. Trees homozygous for both alleles have the pillar appearance (Werner & Chaparro, 2005). In addition, incomplete dominance was observed in br/br/; pl/Pl trees, which exhibit an intermediate phenotype called archer (Werner & Chaparro, 2005). Archer trees are more upright than weeping trees and display only a partial weeping branch appearance (Fig. 2g). This finding suggests that a functional TAC1 gene is required for weeping in peach. Such an interaction points to the intriguing possibility that the vertical orientation in pillar and the rootward orientation in weeping may be caused by changes in the same cellular pathway. 5. Dwarf growth habit Dwarfism is amongst the most common traits observed in nature, and naturally occurring dwarf phenotypes can be found in many tree species. Some dwarf phenotypes found in peach are shown in Fig. 2(h,i) (Scorza et al., 2002; Fideghelli et al., 2003). Dwarfism in plants is typically associated with reduced growth because of shorter internodes – indicating a decreased ability to elongate and/or a reduction in cell division (Ross et al., 2005). Therefore, trees that have a shorter stature because of other physiological changes, such as increased branching or loss of agravitropism (i.e. weeping), are generally not referred to as dwarf. Cultivation of dwarf wheat and rice plants was an important contribution to the green revolution of the 1970s (Ross et al., 2005). The energy in these plants that is normally used for vegetative growth is diverted to reproductive development, enabling higher grain yields supported by thicker and sturdier stems (David & Otsuka, 1994; Peng et al., 1999; Spielmeyer et al., 2002; Nagano et al., 2005). Orchard growers also desire dwarf (Fig. 2h,i) or semi-dwarf (Fig. 2j) trees to minimize orchard maintenance and harvesting/pruning using bucket trucks or ladders (Webster, 2002; Scorza, 2005). To attain this size, growers have traditionally relied on the grafting of scions of commercial cultivars onto naturally dwarfing rootstocks (Webster, 2002; Basile et al., 2007; Tworkoski et al., 2013). Advances in our understanding of the biology behind shoot elongation and overall plant stature could significantly benefit tree-related industries through molecular breeding, chemical treatments or genetic engineering. It has been known since the 1930s that GA has a positive association with shoot elongation, as deficiencies in GA synthesis or signaling can have a dwarfing effect (Brian & Hemmings, 1955; Peng et al., 1999; Spielmeyer et al., 2002). Several studies in poplar, apple and peach have illustrated the critical role of GA in regulating tree size. In poplar, the over-expression of a GA2 oxidase gene, a GA conversion enzyme, reduced the levels of active GA and produced a dwarf tree (Busov et al., 2003). This phenotype was reversed by exogenous application of bioactive GA. Likewise, a Prunus salicina plum with naturally occurring high levels of GA2ox expression and low levels of bioactive GA was found to be dwarf (El-Sharkawy et al., 2012). A study in poplar by Zawaski et al. (2011) showed that No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist over-expression of poplar or bean GA2Ox genes, or the nonfunctioning DELLA genes repressor of GA1-like (rgl) or GA insensitive (gai), led to extreme height reduction and decreased internode lengths. DELLA proteins act to repress GA signaling but, when GA is present, DELLAs are degraded. The rgl and gai mutants, as well as plants over-expressing these alleles, are unable to respond to GA. A gradient in dwarfing severity correlated with the expression levels of the GA2Ox and mutant DELLA transgenes; the higher the expression, the greater the dwarfing effect. Another study by Zhu et al. (2008) reported dwarf phenotypes in three different apple tree varieties that over-expressed an Arabidopsis gai mutant allele. These apple trees had both reduced internode length as well as a reduction in the number of nodes (Zhu et al., 2008). The repression of GA20-oxidase, which causes a reduction in bioactive GA, also produced a dwarf phenotype in apple (Bulley et al., 2005). This dwarfism was reversed by GA application. Combined, the results of these studies provide strong evidence that active GA and functional GA signaling pathways are crucial for internode elongation in trees, and thus regulate overall tree height. Naturally occurring dwarf trees have not yet been associated with mutations in GA biosynthesis or signaling. However, several gene mapping studies have found QTLs associated with dwarfing (Chaparro et al., 1994; Foolad et al., 1995; Dirlewanger et al., 2004). With the increasing use of whole genome sequencing and RNAseq, it is probably only a matter of time until dwarf alleles are identified. Three naturally occurring dwarf architectures in peach have been described previously as distinct monogenic alleles. The brachytic dwarf (dw/dw) peach has short internodes, thick stems and large leaves (Fig. 2h) (Lammerts, 1945; Scorza, 1984). The A72 homozygous dwarf (n/n) has short internodes, small leaves and forked branching (Fig. 2i). The A72 allele also has incomplete dominance; heterozygous A72 trees (n/N) are semi-dwarfs (Fig. 2j) (Monet & Salesses, 1975; Gradziel & Beres, 1993; Hu & Scorza, 2009). Both the brachytic dwarf and the A72 dwarf architectures have altered GA levels and cannot be rescued by the application of GA (R. Scorza, pers. comm.), suggesting a deficiency in GA perception or signaling. Although the gene has not yet been identified, the dw mutation was first mapped to peach linkage group 5 from a peach 9 almond hybrid (Foolad et al., 1995), and later to linkage group 6 of an interspecies Prunus reference map (Dirlewanger et al., 2004). The A72 dwarf allele has not been mapped. The third reported peach dwarf, Dwarf3 (dw3), has thin stems and willowy growth, and has been linked to the wavy leaf (Wa) locus (Chaparro et al., 1994). In addition to GA, other hormones have also been linked to dwarfism. Like GA, BRs are also obligatory for growth (Ross et al., 2005). Numerous BR-deficient Arabidopsis, pea and tomato mutants are abnormally short because of reduced cell elongation and/or division (Busov et al., 2008). To date, there have been very few experimental results connecting dwarf trees to BR biosynthesis or response mutants. Pereira-Netto et al. (2009) have shown that application of BR and BR inhibitors to Malus prunifolia (an apple species used for rootstocks) differentially affected lateral and primary shoots through alterations of elongation as well as apical dominance. This indicates that the alteration of BR pathways may enable the generation of dwarf No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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trees, and that naturally occurring dwarfs may in some instances result from impaired BR responses. Abscisic acid (ABA) is most commonly known as a stress response hormone, but can also be a negative regulator of tree growth. Poplar trees rendered insensitive to ABA by expression of the Arabidopsis mutant abi allele developed elongated shoots (Arend et al., 2009). Surprisingly, these poplars did not have higher levels of active GA, indicating that the elongation was not a result of GA induction, but they produced higher levels of ethylene than normal (Arend et al., 2009). Inhibition of the ethylene response reverted the trees to normal growth. The authors concluded that, under normal conditions, ABA acts as an inhibitor of shoot elongation by repressing ethylene responses. Alteration of the timing of floral development by the overexpression of floral meristem development genes can also affect plant stature. Over-expression of APETALA1 (AP1) in birch trees led to both early flowering and a c. 40% reduction in height compared with wild-type trees (Huang et al., 2014). Likewise, AP1 over-expression in tobacco produced shorter plants, and overexpression of FLOWERING TIME 1 in plums led to dwarfism together with other abnormalities (Srinivasan et al., 2012). One possible reason for these findings is that precocious flowering may leave fewer resources for vegetative growth, resulting in decreased height. Alternatively, mis-expression of these flowering genes may alter hormone distribution and/or action in a way that impairs vegetative growth. Flavonoids, which decrease auxin transport ability, may also be involved in the regulation of tree size. Apple trees with reduced expression of three Chalcone Synthase (CHS) genes had shortened internodes and grew more slowly than standard apples (You et al., 2014). CHS genes code for enzymes in the phenylpropanoid pathway, the first committed step of flavonoid synthesis, and CHS knock-down apples showed decreased levels of flavonoids. The size of fruit and nut trees is often controlled using what are termed dwarfing rootstocks. When grafted onto certain rootstocks from either the same or different tree species, scion growth becomes stunted, resulting in a dwarf or semi-dwarf phenotype. Although the specific mechanisms by which rootstocks exert their dwarfing affect is not fully understood, a handful of studies have linked the effects to changes in hormones or hormone signaling. Prassinos et al. (2009) found differential gene expression between dwarfing rootstocks and scions that code for BR signaling and the metabolism of flavonoids. Aloni et al. (2010) suggested that dwarfing from rootstocks is a result of reduced rootward auxin transport resulting in increased CK levels. As a result of the relatively small number of naturally dwarfing rootstocks available and their variable effectiveness, transgenic dwarfing rootstocks are being developed. One example is the dwarfing ability of apple rootstock over-expressing the Rooting Locus B (RolB) gene from Agrobacterium rhizogenes that stimulates rooting (Smolka et al., 2010). 6. Compact The compact growth habit, in general, is associated with trees that have a smaller and more condensed stature than normal. Two wellNew Phytologist (2015) 206: 541–556 www.newphytologist.com

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described compact trees are the compact peach (Fig. 2k) and the compact apple. Although these two trees are both described as being ‘compact’ compared with their standard growth habit, their actual shoot architectures are different. Compact cherry, pear and plum trees, which were developed from induced mutagenesis, have architecture similar to the compact apple, which resembles a semidwarf growth habit (Fideghelli et al., 2003). The compact peach growth habit arose from a bud mutation in the peach cultivar Redhaven (Van Well, 1974). These compact trees have wider branch angles, longer branches, shorter internodes, profuse lateral branching (suggesting weak apical dominance) and smaller but more numerous leaves compared with the standard peach (Fig. 2a,k) (Van Well, 1974; Scorza et al., 1984, 1999; Mehlenbacher & Scorza, 1986). These characteristics result in a dense canopy with reduced light penetration, which is undesirable for fruit production because of the need for excessive pruning (Scorza et al., 1999, 2002). The compact peach phenotype has a Mendelian segregation pattern consistent with a single dominant allele, ct (Mehlenbacher & Scorza, 1986; Scorza et al., 2002). The ct allele has not yet been identified or mapped. The tree phenotype suggests that the causative allele may interfere with branching inhibition, indicating that the gene may be involved in SL biosynthesis or SL signaling. As mentioned earlier, herbaceous plants with impairments in the SL pathway have a high degree of branching and a bushy appearance similar to the peach compact tree (Gomez-Roldan et al., 2008). In contrast with the compact peach, the compact apple architecture more closely resembles a semi-dwarf-type tree. Compact apple trees have reduced size, upright growth, short internodes, fewer and thicker lateral shoots, smaller and thicker leaves, and greater reproductive than vegetative growth, resulting in high yields of fruit (Lapins, 1969b; Webster, 2002; Fideghelli et al., 2003). Blazek (1983) studied the segregation of a compact apple cultivar and determined that it was under the control of a single recessive gene which was also influenced by additional modifying genes. The lack of excessive branching associated with the compact apple phenotype suggests that it is not likely to be an abnormality associated with SL biosynthesis or signaling. Rather, it may be related to the GA pathway (as suggested by thicker shoots and short internodes) and/or post-transcriptional regulation mechanisms (as in the columnar apple, which has fewer and upright branches). The compact apple growth habit has developed naturally in a Delicious cultivar (Lapins, 1965). However, some compact McIntosh, Spartan and Golden Delicious cultivars originated from irradiated scions as part of the apple breeding program (Lapins, 1965, 1969b; McIntosh & Lapins, 1966). Although little is known about the molecular control of tree branching propensity, naturally occurring compact mutants offer opportunities to dissect this process, and may serve as a starting point to unravel the primary molecular and genetic control mechanisms.

plant height, degree of branching, branching angles, pattern of flowering, wood composition, sink–source relationships, hydraulic conductance of vascular tissues and shoot growth orientation. Most of the developmental processes that control these components have been described to at least some extent in model plant systems. Most, if not all, of these processes involve the movement and perception of distinct plant hormones and/or other signals, such as sugars. Thus, genetic changes that alter hormone synthesis, regulation, perception or signaling have the potential to induce changes in tree architecture. The identification of genes involved in branch orientation, degree of branching, tree size, flowering and reaction wood formation should aid the development of superior tree varieties across diverse agricultural, forestry and landscaping industries. The modulation of the genes involved in maintaining active GA and in GA response may be a promising method for limiting the size or branch orientations of agriculturally important fruit and nut trees. Simple modifications of TAC1, LAZY1 and Pl may be useful for developing trees with branches having optimized orientations. For example, apple trees exhibiting horizontally oriented branches, similar to those trained by the espalier method, may be advantageous for automatic harvesting and reduced pruning. By contrast, fastigiated poplar trees with very few lateral branches may be useful for high-density timber production. Deciphering the genes that are associated with the compact peach may also aid in the development of trees with more or fewer branches. Lastly, understanding how branch orientation influences wood chemistry could be valuable to the pulp and biofuel industries. Significant progress is now being made in deciphering the molecular causes behind genetically predetermined tree architectures in angiosperms. Although the roles of individual hormones in various aspects of plant development are becoming clear, their specific mechanisms of action and how they interact with each other remain poorly understood. Moreover, an understanding of how environmental conditions influence the temporal and spatial hormonal control of tree architecture is also lacking, as is an understanding of the hormonal control of vegetative and reproductive growth which strongly impacts tree structure. Sink–source relationships within vascular tissue, together with hydraulics and structural constraints, have also been implicated in determining overall plant architecture, but few, if any, genetic studies have been reported for such traits. For example, little is known about the molecular mechanisms by which sink–source relationships influence stem diameter, a phenomenon that has been successfully described by the pipe model theory (Shinozaki et al., 1964a,b). Future research in these areas will aid in efforts to optimize tree architectures for agricultural and forestry purposes, and will increase our understanding of shoot growth development in all plants.

Acknowledgements V. Conclusions The overall molecular and genetic programming that regulates tree architecture is very complex. There are multiple structural components that make up the growth habits of trees, including New Phytologist (2015) 206: 541–556 www.newphytologist.com

The authors would like to acknowledge the researchers whose contributions to this field we were unable to cite as a result of spatial constraints. In addition, we are indebted to our reviewers for extremely helpful comments that significantly improved the quality No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist and content of the paper. We also thank Dr Tom Tworkoski for his insight and discussion on apple tree architecture, and Dr Ralph Scorza for helpful suggestions and edits of the manuscript. This work was supported by Agriculture and Food Research Initiative competitive grant 10891264 from the USDA National Institute of Food and Agriculture.

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