Following the star: Inflorescence heliotropism

Accepted Manuscript Title: Following the star: inflorescence heliotropism Authors: Alejandro M. Serrano, Maria Verónica Arana, Lucas Vanhaelewyn, Carlos L. Ballaré, Dominique Van Der Straeten, Filip Vandenbussche PII: DOI: Reference: S0098-8472(17)30280-0 https://doi.org/10.1016/j.envexpbot.2017.11.007 EEB 3331 To appear in: Environmental and Experimental Botany Received date: Revised date: Accepted date: 16-10-2017 14-11-2017 14-11-2017 Please cite this article as: Serrano, Alejandro M., Arana, Maria Verónica, Vanhaelewyn, Lucas, Ballaré, Carlos L., Van Der Straeten, Dominique, Vandenbussche, Filip, Following the star: inflorescence heliotropism.Environmental and Experimental Botany https://doi.org/10.1016/j.envexpbot.2017.11.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Title: Following the star: inflorescence heliotropism 1,2 , Maria Verónica Arana 1,3 , Lucas Vanhaelewyn4, Carlos L. Ballaré1,5, PT Authors: Alejandro M. Serrano RI Dominique Van Der Straeten 4, Filip Vandenbussche 4 CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas)-Argentina 2 IADIZA, Av. Ruiz Leal s/n Parque Gral. San Martín, Casilla de Correo 507, Mendoza 5500, Argentina 3 INTA, Modesta Victoria 4450 - Valle Verde, Bariloche 8400, Rio Negro, Argentina 4 Laboratory of Functional Plant Biology, Department of Biology, Ghent University, KL Ledeganckstraat 35, N U SC 1 A B-9000 Gent, Belgium 5 M IFEVA Universidad de Buenos Aires, Ave. San Martín 4453, C1417DSE, Buenos Aires, Argentina and IIIB- INTECH, Universidad Nacional de San Martín, B1650HMP Buenos Aires, Argentina D Corresponding author: Filip Vandenbussche, Laboratory of Functional Plant Biology, Department of CC EP Tel: +32 9 264 5186 TE Biology, Ghent University, KL Ledeganckstraat 35, B-9000 Gent, Belgium. Filip.Vandenbussche@ugent.be. A Highlights  Different types of heliotropism can be characterized by mechanistic, spatial and/or temporal specification.  Heliotropism of reproductive structures is widespread in the plant kingdom.  Physiological mechanisms of inflorescence heliotropism depend on hormonal responses (seasonal heliotropism -Arabidopsis) or a combination with regulation by the circadian clock (diurnal heliotropism -sunflower).  Flower heliotropism is closely associated with entomophilous pollination, and increased reproductive success due to heliotropism frequently depends on the consequent establishment of a temperature optimum for pollinators or plant physiological processes. ABSTRACT Plant movements in response to directional solar radiation, known as "heliotropism" are frequently observed in nature. Although there is a considerable amount of literature on these movements in vegetative organs, knowledge about heliotropic responses in flowers and inflorescences is relatively PT limited. Here we comprehensively review studies on this topic, profile the diversity of responses RI encompassed under the term "heliotropism" and propose a conceptual framework for their classification. In addition, we discuss the mechanisms underlying different types of heliotropism in two species SC commonly used as model systems: Arabidopsis and sunflower. Finally, the ecological consequences of U floral heliotropism are elaborated with an emphasis on the effects on plant reproductive success, and the N potential agricultural implications of manipulating heliotropic responses are addressed as well. We A conclude that inflorescence heliotropism appears conserved in many plant species that depend on M pollinators, and consists of an auxin dependent response to solar radiation. TE Auxin; Pollination; Fitness D Key-words: Heliotropism; Phototropism; Flowers; Inflorescences; Arabidopsis; Sunflower; Phototropins; CC EP 1. INTRODUCTION Life on the Earth’s surface is exposed to solar radiation, which constitutes a crucial source of energy for photosynthesis, heat for the regulation of metabolic processes and information from which A plants can detect spatial and temporal features of their environment. In this context, plants in the field can be spotted frequently with flowers facing the sun (Fig. 1), and in many studies, researchers have asked how and why such orientation occurs. The movements of plant organs in response to the incident solar light are encompassed under the term “heliotropism”, which derives from the Greek “helios” (sun) and “tropos” (turn). Although there is a large body of literature about plant movements in response to light, knowledge on movements of flowers or inflorescences is limited compared to that on the responses shown by vegetative organs. Both heliotropic and phototropic responses of vegetative organs have been extensively reviewed elsewhere (Whippo & Hangarter 2006; Pedmale et al. 2010; Koller 2011; Hohm et al. 2013) and will not be considered PT in the present article. The main objective of this paper is to critically review the existing literature on flower RI and inflorescence orientation in response to directional light. We review studies in which heliotropic responses in flowers have been assessed, and attempt to produce a general framework organizing the SC existing literature on the topic. We then present our current knowledge of mechanisms involved in U inflorescence and flower orientation, and assess the ecological and potential agronomic implications of A N flower heliotropism. M 2. CONCEPTUAL FRAMEWORK FOR THE CLASSIFICATION AND UNDERSTANDING OF HELIOTROPIC RESPONSES D An important issue that arises when trying to compare studies on inflorescence heliotropism is TE that no specific criteria are established to discriminate between different types of heliotropic movements and no protocol exists to standardize the way of measuring and quantifying the response. Because of that, CC EP many studies use the same term “heliotropism” to describe different responses, or conversely, describe the same response using different terminology. Therefore, it is necessary to establish clear definitions of A heliotropism and related terms (see Box1). 2.1. Mechanistic specification of heliotropism: growth-mediated, turgor-mediated, and circadian controlled movements Closely related to heliotropism is a process known as phototropism, from the Greek “phos” (light; genitive “photos”) and “tropos” (turn). As it has been stated by Sherry & Galen (1998), the difference between both concepts is often difficult to establish. This is shown in several examples, where phototropism is considered indeed as a special case of heliotropism, in which the light source is fixed in space (Kevan 1972; Hart 1990; Zhang et al. 2010). The term “phototropism” often refers to the differential growth or expansion of plant tissues in response to the direction of incoming light, which generates an PT orientation response. Furthermore, on many occasions the phototropism concept is constrained to RI movement toward the light, induced by light of wavelengths shorter than 500 nm (UV-Blue) and its mechanism has been mostly associated to the action of a transmissible substance, auxin (Whippo & SC Hangarter 2006). U In contrast to phototropism, the use of the term heliotropism is not linked to any particular N mechanism. Therefore, the term “heliotropism” is often applied to any kind of plant movement that leads A to orientation of an organ in response to the direction of the sun, regardless of the mechanism that drives M that movement. In literature one can frequently encounter studies that use the term heliotropism to refer to movements that are driven either by differential growth or by turgor changes in specialized cells at the D base of the leaves (pulvini). TE Circadian rhythms can also take part in the mechanism of heliotropic responses. For example, in sunflower, a circadian mechanism re-orients the inflorescences during the night (Atamian et al. 2016), CC EP essentially generating a heliotropic response when the sun is not visible. In the particular case of the movement of sunflower heads, it has been recently demonstrated how phototropic and circadian A processes contribute to the full heliotropic response of unopened flower heads (Atamian et al. 2016). 2.2. Spatial specification of heliotropism: Vertical and Horizontal Heliotropism. When describing quantitatively heliotropic movements, it is necessary to determine to which extent the organ tracks the sun; in other words, the magnitude of the heliotropic response is associated with the angle between the direction of sun rays and the direction to where the organ points. There is a high variability among studies regarding the criteria applied to choose parameters for quantifying heliotropism (Fig. 2). Below we suggest a series of terms to distinguish between the aforementioned criteria.  Horizontal deviation from the sun: the angle between the flower and the solar position measured in the horizontal plane parallel to the earth surface (Kevan 1972; Luzar & Gottsberger 2001; Fig. PT 2a). The use of this variable is advisable when elevation of the sun is rather stable, like for studies  RI in the arctic. Vertical deviation from the sun: the angle between the flower and the solar position measured SC along the vertical plane, parallel to the gravity vector (Stanton & Galen 1993; Zhang et al. 2010; U Fig. 2b). This variable is suitable for studies where the light source is not too variable in trajectory, Absolute deviation from the sun: a three dimensional magnitude that integrates both vertical and A  N like for example, phototropic movements towards a fixed light source. M horizontal components of the angular deviation from the sun. The angle is calculated from the shadow projected by a heliotropometer consisting of a white disc and a stick normal to the corolla D (Stanton & Galen 1989; Totland 1996; Fig. 2c). This approach is useful when there is no need to  TE specify the azimuthal (horizontal) or elevation (vertical) components of the angle. Horizontal deviation from the east: the angle between the flower orientation and the geographic CC EP east measured along the earth surface (horizontal plane), (Stanton & Galen 1989; Zhang et al. 2010; Fig. 2d). This is used as an alternative to the horizontal deviation from the sun, when there is an intention to trace the trajectory of the flower throughout the day as a continuously increasing A magnitude and it is easily translatable to the horizontal deviation from the sun for comparison purposes.  Vertical orientation toward the east/west: consists in measuring the elevation angle of the flower above the horizon, applying a distinction between east and west orientation using either a positive or negative criterion (Lang & Begg 1979), or values lower or higher than 90° (Vandenbrink et al. 2014) (Fig. 2e). This procedure is only advisable in low latitudes where the apparent trajectory of the sun goes from east to west passing close to the zenith at noon The above descriptions illustrate the variety of perspectives from which heliotropism is analyzed, and highlights the importance of being cautious when making comparisons between different cases of 2.3. Temporal specification of heliotropism: Diurnal vs. Seasonal RI PT heliotropism. SC It is generally assumed that heliotropism implies a daily movement of plant organs tracking the U solar trajectory in periods of approximately 24 h. In 2002, Patiño et al. described the floral movement of N two tropical convolvulaceous species and noted that the short lived flowers preferentially oriented toward A the north before the equinox and toward the south after the equinox. Although these flowers did not show M daily east to west movements, they were considered heliotropic because their orientation followed the predominant position of the sun in each part of the year. Therefore, Patiño et al. (2002) called this type of D heliotropism “seasonal heliotropism”, in contraposition to more familiar “diurnal heliotropism”. It is TE possible that plants that have this type of heliotropism may have been considered as non-heliotropic or simply ignored in previous studies. CC EP In Fig. 3, we summarized the data available in literature on horizontal heliotropism for several species (Kevan 1972; Stanton & Galen 1989; Totland 1996; Luzar & Gottsberger 2001; Patiño et al. 2002; Zhang et al. 2010), and compared their observed behavior with that of ideal flowers showing perfect daily A and perfect seasonal heliotropism. Heliotropic responses were quantified as the absolute value of the deviation of flower orientation from the azimuthal position of the sun during the day. Perfect daily heliotropism (of an ideal plant) consists of a situation where there is an absolute alignment of the flower and the sun (values equal to zero) at all times, while an ideal, perfect seasonal heliotropism was recognized as a case where a flower points to the equator, at a fixed angle throughout the photoperiod. To date, with the exception of Ipomoea pes-caprae (Fig. 3c), studied by Patiño et al. (2002), most species have been considered heliotropic in the traditional, diurnal sense. Nevertheless, a careful analysis of the movements shown by these plants reveals that most of them may be considered being seasonallyrather than diurnally-heliotropic. For example, the curves describing the movements of Dryas integrifolia PT and Ranunculus acris in the Arctic (Fig. 3a) are much closer to the reference line corresponding to seasonal RI heliotropism than to the curve representing diurnal heliotropism. In mountainous areas, Anemone rivularis constitutes another example of seasonal heliotropism and Ranunculus montanus a case of diurnal SC heliotropism with an average lag of 30° (as can be inferred from a rather flat distribution of points around U an angle of 30°) (Fig. 3b). Ranunculus adoneus shows an intermediate response, i.e. tracking the sun in the A N morning (until 10 a.m.) and staying in a fixed position during the afternoon. M 3. BIOLOGICAL DIVERSITY OF THE INFLORESCENCE HELIOTROPIC RESPONSES In vascular plants, heliotropism and phototropism of vegetative organs has been described in D hundreds of species (Ehleringer & Forseth 1980; Sailaja & Rama Das 1996; Iino 2001), while floral TE heliotropism has been reported in 94 species, belonging to 28 families occurring in extremely different biogeographical areas, i.e. from cold Arctic (Kevan 1973; Mølgaard 1989; among others) to temperate and CC EP warm equatorial regions (Smith 1975; Patiño et al. 2002; among others) (Table 1). Moreover, among the species that are currently documented to be heliotropic, detailed quantification of the response is only available for 12 of them in terms of the duration of the sun-tracking behavior, and for 7 of them in terms A of the orientation angle of the flowers (Table 1). Phototropic behavior of reproductive organs is widespread, and occurs even in fungi and lower plant taxa such as Phycomyces (Fungi, Mucoraceae) sporangiophores (Denisson 1965), Pellia epiphylla (Bryophyta - Pelliaceae) sporophyte setae (Thomas et al. 1987), Aplodon wormskioldii (Bryophyta - Splachnaceae) sporophytes (Steere 1973) and conchosporangia of the marine red macroalga Pyropia yezoensis (Rhodophyta - Bangiaceae) (Takahashi & Mikami 2016). A special case of seasonal heliotropism can be found in columnar cacti native from desert and semi-arid lands of South and North America and is called stem tilting. Many species of columnar cacti show PT a conspicuous bending of their upper section toward the equator (i.e. to the South in North American RI deserts and to the north in southern regions). This case of differential growth in the stem results eventually in an orientation toward the sun of the part of the plant where flowers develop. In some species of the SC genus Copiapoa which grow in the cold Atacama desert, this apical part of the body is covered by a waxy U reflective layer and a dense hairy area in the central meristematic region, corresponding with the location N of the flowers. As a result of this stem tilting, the well protected apex of the column becomes the warmest A part of the cactus, minimizing the lateral, glabrous surface exposed to solar radiation during the dry and M warm part of the year. At the same time, the flowers are heated during the cool months when flowering occurs (Ehleringer et al. 1980). In a warm desert in an intertropical region of Mexico, the same equatorial D tilting can be observed, but in this case, the south oriented apices of the columnar Echinocactus TE platyacanthus provide protection from overheating to the flowers that develop in the warm summer when the sun shines slightly from the north, while during the rest of the year, light interception is maximized CC EP (Herce et al. 2013). In contrast, negative stem tilting has been reported in Cephalocereus columna-trajani, a giant cactus of Zapotitlán, Mexico (Zavala-Hurtado et al. 1998), but due to the south orientation of the sun during the flowering season, the same double consequences of protection of reproductive structures A against heat load, and maximization of annual radiation interception is achieved. In the above mentioned datasets, most reports on flower and inflorescence heliotropism describe orientation toward the light. However, in certain species, inflorescences bend away from the light, thus displaying negative heliotropism. For instance, in the vines Cymbalaria muralis (Linaria cymbalaria) (Schmitt 1922) and Tropaeolum majus (Oehlkers 1922) the negative phototropism occurs after fertilization and this has been interpreted as an adaptation to increase the chances of the seeds to fall on rocks or wall surfaces, which are suitable places for seedling establishment (Junghans & Fischer 2008). Change in tropic direction of the inflorescence appears somewhat more general, as it was also observed in Cyclamen persicum (Darwin 1880). The latter system was investigated more thoroughly in Cyclamen, and in PT accordance with the observations in Cymbalaria and Tropoaelum, young inflorescence stems are positively RI phototropic, while older, fruit baring stems, display negative phototropism (Kiendl 1940; Zinsmeister SC 1960). U 4. CANDIDATE PHYSIOLOGICAL MECHANISMS FOR THE DIFFERENT HELIOTROPIC RESPONSES N Our understanding of the mechanisms that underlie tropic responses in vegetative organs is A substantially greater (especially in hypocotyls or coleoptiles of young seedlings) than in flowers or M inflorescences. To date, two classes of mechanisms for tropic movements have been described for plants, irrespective of the organ: hormone (auxin) based, and turgor (pulvinus) based responses. The pulvinus is D a specialized structure typically found on leaves, leaflets or petioles, and to date no turgor-based TE mechanism has been described for inflorescence or flower heliotropism. Current knowledge indicates that heliotropism of flowers is the result of differential growth of pedicel, peduncle or the entire stem of the CC EP plant. Few studies are available that reveal details on the mechanism of inflorescence movements. Most of our mechanistic understanding is derived from work with two model systems: sunflower, where solar A tracking of the unopened flower heads has been studied in detail (Atamian et al. 2016; Kutschera & Briggs 2016), and Arabidopsis, in which multiple molecular genetic tools have been used to unravel the mechanisms of phototropism in inflorescence stems (Kumar & Kiss 2006; Kagawa et al. 2009; Kumar et al. 2011; Sato et al. 2014). 4.1. Sunflower buds: a model for diurnal heliotropism Solar tracking in sunflowers depends on differential elongation of the stem. During the day the east-facing side elongates faster than the west-facing side, and this pattern of differential elongation is reversed during the night (Atamian et al. 2016). The diurnal differential growth persists in free running PT conditions, indicating that it is under control of the circadian clock (Fig. 4a). An “east-west” moving blue RI light source, with 16h light /8h dark containing periods, is sufficient to mimic the response in the field, while this is not the case for a 30h (20h blue light/10h dark) period. Hence, directional blue light SC photoreceptors, like phototropins, are believed to act in concert with the circadian clock to control U downstream growth regulating processes (Vandenbrink et al. 2014; Atamian et al. 2016). It is of note that N the circadian clock itself can be under the control of multiple photoreceptors (Millar 2003), which all may A have an effect on the outcome of solar tracking. The differential growth pattern is associated with M differential expression of distinct auxin response genes at the faster elongating side, which points to the necessity of auxin signaling in the elongating tissue. Furthermore, elongation in sunflower stems depends D on the presence of the plant hormone gibberellin. In view of the reported interactions between auxins and TE gibberellins in other species (Ross et al. 2003; Weston et al. 2009; Willige et al. 2011), a similar interplay may cause bending in differential growth of sunflower stems. Both hormones are necessary for a correct CC EP elongation of cells, and often have synergistic effects. Older sunflowers lose the ability to elongate in a western direction, resulting in east facing heads. The mechanism behind this appears to depend on a combination of circadian gating conferring a higher sensitivity to phototropic signals in the morning, and A a gradual cessation of elongation growth of the stem (Atamian et al. 2016). 4.2. Arabidopsis: a model for seasonal heliotropism? The Arabidopsis inflorescence has no record of tracking the sun in the diurnal way sunflower buds do, but rather classifies as seasonally heliotropic (Serrano and Arana, unpublished). However, a substantial amount of mechanistic data is available on the response of inflorescences to artificial light sources in controlled conditions. Multiple photoreceptors appear to be involved in the phototropic response of Arabidopsis inflorescence stems toward blue light (Fig. 4). Analogous to the situation in seedlings, the blue light photoreceptors phototropins induce the movement of inflorescence stems of Arabidopsis toward PT blue in a very sensitive manner (Kagawa et al. 2009). Interestingly, in similar blue light conditions, the red- RI far red photoreceptor phytochrome E (phyE) has been suggested as an additional important photoreceptor for phototropism in inflorescence stems (Kumar & Kiss 2006). Auxins appear involved in SC inflorescence phototropism, as the dominant Arabidopsis AUX/IAA7 mutant axr2, which shows an auxin U resistant phenotype, lacks positive inflorescence phototropism and even tends to show negative N phototropism (Sato et al. 2014). This suggests that correct auxin signaling is of utmost importance to A achieve the inflorescence phototropic response. Furthermore, auxin efflux carrier abcb19 (mdr1) mutants M have enhanced phototropism towards blue light (Kumar et al. 2011). Current models indicate that ABCB19 is responsible for the downward flow of auxins from apical D meristem to base, in both seedlings and inflorescence stems (Noh et al. 2001). Inferring that a similar TE model applies to both seedlings and inflorescence stems, it is tempting to speculate that apically derived auxin diminishes the capacity of inflorescences to respond in a phototropic manner. Since auxin signaling CC EP is necessary for bending, it is likely that with diminished downward auxin transport, the eventual auxin available in the bending zone becomes closer to the thresholds necessary for efficiently generating an auxin gradient and consequent differential growth (Vandenbussche et al. 2014). In such a case, the locally A available transport machinery for generating a lateral auxin gradient (Cholodny-Went theory) may be more effective than when a strong downward auxin flow is present (Fig . 4). Similarly to what is known for Arabidopsis, blue light has been shown more effective than light of higher wavelengths for inducing heliotropism in other species such as Ranunculus adoneus (Stanton & Galen 1993) and Anemone rivularis (Zhang et al. 2010). Furthermore in both studies it was shown that a mechanism based on differential growth rates between shaded vs. illuminated sides of the peduncles is responsible for the bending response. Finally, different floral organs have been identified as important components of the heliotropic mechanism in plants growing in the wild. For example, flowers of Dryas integrifolia lacking the gynoecium RI Papaver radicatum and Anemone rivularis (Corbett et al. 1992; Zhang et al. 2010). PT lost the response (Krannitz 1996) while petals and tepals are required for heliotropic movements of Future challenges to unravel the mechanistic differences between diurnal and seasonal SC heliotropism lie ahead. In this respect, the investigation of differential involvement of components of the A N targeted mutagenesis strategies, will be of key importance. U circadian clock in diurnally versus seasonally heliotropic species, with the help of currently available M 5. ECOLOGICAL SIGNIFICANCE Solar light provides not only energy for photosynthesis but also information about the D characteristics of the environment, mainly associated to competition and interactions with the animal TE kingdom. In addition, the infrared portion of the solar spectrum constitutes a source of heat. In this context, phototropism of vegetative organs allows plants to orient their photosynthetic tissues according CC EP to incoming light, increasing light interception in photosynthetic organs. However, the same phenomenon taking place in organs of which the primary task is not photosynthesis related, like flowers, cannot be explained by the same principles of light capture with a subsequent increase in photosynthetic metabolism A and growth. In spite of the aforementioned diversity of plant heliotropic responses, ecological studies indicate that heliotropism has a major and unique consequence in the plant kingdom; the increment of reproductive success. This is reflected in different processes that extend from the maturation and development of sexual structures to the success of pollination and the contribution to the number / weight of the seeds (Table 2). 5.1. Effects of flower heliotropism on floral characteristics and its relation with entomophillous pollination Most of the ecological studies point to a positive effect of floral heliotropism on entomophillous PT pollination. From a general point of view, orientation of flowers towards the light may help in displaying RI them for pollinators, thus generating more contrast with the background vegetation. Flower color itself may also be influenced by the position of the flower vis à vis the light. Although in many species much of SC the floral pigmentation is developmentally regulated, and patterns are formed in the bud (Schlangen et al. U 2009), the color of flowers is affected by environmental cues (Griesbach 1987). The presence of sufficient N light is necessary for pigmentation of petals of some Rhododendron species (Halligan 1988), or for A intensifying color of flowers of species such as Paeonia lactiflora (Zhao et al. 2012) and Eustoma M grandiflorum (Griesbach 1992; Zhao and Tao, 2015). The latter species has been reported to have a clearly phototropic flowering stem (Scace, 2001), but for other species the correlation between heliotropism and D light induced color changes has not been investigated. It is plausible that such promotion of color intensity TE or pattern by light, influences the visiting behavior of pollinators that are attracted by the pigment based floral characteristics (Chittka & Raine 2006). For instance, bees use the contrast of flower color versus a CC EP green background to detect flowers (Spaethe et al. 2001; Chittka & Raine 2006) and for attracting pollinators numerous plant species rely at least in part on light absorbance or reflectance (Chittka et al. 1994; Horth et al. 2014; Koski & Ashman 2014; Peterson et al. 2015). Within a species, floral color can vary A and differences occur in the patterns that serve as guide to pollinators (Yoshioka et al. 2005; Horth et al. 2014). In this context it is noteworthy that wild bees prefer exaggerated large size floral guides, suggesting benefits for pollination (Horth et al. 2014). Nevertheless, despite these possible influences on floral display, in most cases entomophillous pollination was found predominantly associated with an increment of the temperature in heliotropic flowers with a consequent creation of a favorable environment for insect activities and has led to the adoption of the so-called heat reward hypothesis. This might represent a plant-pollinator co-adaptation, of particular relevance in cold artic and alpine ecosystems (Kevan 1975; Smith 1975; Stanton & Galen 1989). On the other hand, the increment of floral temperature increases the production of nectar PT (Petanidou & Smets 1996) or other botanical characteristics (Cooley 1995) that might promote the visiting RI by pollinators. It has been demonstrated that an increase in flower temperature as well as the light irradiation itself also enhances the release of volatile components (Jakobsen & Olsen 1994; Hu et al. 2013; SC Borghi et al. 2017) and influences the relative abundance of the different floral scent constituents (Farré- U Armengol et al. 2014) by modifying several plant physiological processes involved at different stages of N the biosynthesis of volatile components and their emission or release (Niinemets et al. 2004), or by A affecting the physicochemical properties of the substances (volatility, diffusivity, etc). However, the M release of floral scents decays after an optimal temperature is reached. This optimal temperature for volatile compound emission varies across plant species according to the conditions that are predominant D during flowering time; i.e winter-flowering species show the lowest optimal temperature while summer- TE flowering species have the highest (Farré-Armengol et al. 2015). For this reason, it was proposed that extreme warming such as predicted for global average temperatures at the end of the century may cause CC EP a significant disruption of this kind of plant-pollinator communication. Observations by Kevan (1970) at Hazen Camp (North Canada) indicated that mosquitoes and dance flies may rise their body temperature up to 14°C above ambient air by resting for long periods inside A flowers of Dryas integrifolia. Smith (1975), Stanton & Galen (1989) and Luzar & Gottsberger (2001), also measured the time spent by pollinators inside heliotropic versus non-heliotropic flowers and observed that insects spent more time in heliotropic ones. Studies in sunflower heads showed that heliotropic inflorescences facing east in the morning attracted five times more pollinators than inflorescences artificially oriented to the west. This effect was correlated with higher temperatures in east oriented heads. Moreover, artificially warmed inflorescences pointing west, also attracted more pollinators than non-heated inflorescences, when both groups of inflorescences were equally oriented (Atamian et al. 2016). However, the authors could not fully explain the effect of inflorescence temperature in the number of visits, since artificially warmed heads facing west indeed received more visits than cooler ones, yet less PT than naturally east-oriented heads, suggesting additional plant-pollinator interaction mechanisms play a RI role. Other examples of flowers that become more attractive for pollinators as a result of their SC heliotropic response include Oritrophium limnophylum (Smith 1975), Ranunculus montanus (Luzar & U Gottsberger 2001), Ranunculus adoneus (Stanton & Galen 1989) and Adonis ramosa (Kudo 1995). N Interestingly, in the tropical species Merremia bornensis, heliotropic flowers are colder than non- A heliotropic ones. Notwithstanding this, heliotropic flowers receive more pollinator visits. Here heliotropic M orientation of flowers and transpiration are proposed to prevent high temperatures of the gynoecium (Patiño et al. 2002), and may be a variation on the theme of achieving the optimal temperature conditions D for pollinators. On the other hand, no significant effects in pollination of flower heliotropism of Drosera TE filiformis flowers have been detected, suggesting an evolutionary anachronism that no longer has a CC EP function (Wilson 1994). 5.2. Effect of flower heliotropism on plant physiological processes related to reproductive success In addition to its effect on the attraction of pollinators, changes in floral temperature due to A heliotropism may create a favorable thermic environment for the development of plant physiological processes related to sexual reproduction. For example, the duration of meiotic division of pollen mother cells, pollen maturation, pollen transfer, stigmatic receptivity, pollen germination, pollen tube growth, double fertilization and ovule and seed development are all processes regulated by temperature (Pigott & Huntley 1981; Kjellberg et al. 1982; Young 1984; Corbet 1990; Stephenson et al. 1992; Kudo 1995; Delph et al. 1998; Hedhly et al. 2003; Li & Huang 2009; Whittle et al. 2009) and might be affected by thermic environments created by heliotropism. In accordance with this, flower heliotropism of Anemone rivularis increased flower temperature, seed size and number and it was suggested that flower heliotropism enhances the pollen viability and seed production, resulting in higher reproductive success (Zhang et al. PT 2010). RI Heliotropism has been shown to increase seed set in Papaver radicatum (Corbett et al. 1992), Anemone rivularis (Zhang et al. 2010) and Ranunculus adoneus (Stanton & Galen 1989). In addition, SC heliotropic flowers of Papaver radicatum and Dryas integrifolia produced heavier seeds than non- U heliotropic flowers (Corbett et al. 1992; Krannitz 1996). Such effects may relate to the light reaching the N embryo during seed filling. Although to date not (yet) associated with heliotropism, light stimulates A photosynthesis in embryos of Brassica, and thus affects oil content in oilseed rape (Asokanthan et al. 1997; M Goffman et al. 2005). Furthermore, in soybean, seed filling and thus yield are dependent on the light regimes reaching the developing embryo (Allen et al. 2009). D On the other hand, within the frame of global warming, it is important to consider that some TE heliotropic flowers, particularly those growing in warm environments, may become damaged if temperatures rise to stressful conditions. For example, it has been proven that heat stress reduces fruit CC EP number and weight in tomato and seed number per fruit (Peet et al. 2002). Moreover, solar-tracking flowers of Ranunculus adoneus, experience higher rates of water loss due to transpiration, and absorb a larger amount of water from the soil than non-heliotropic flowers (Galen 2006). Hence it was suggested A that flower heliotropism rises the water cost of reproduction, meaning that a potential trade-off relation between water use and flower behavior as that of heliotropism may shape the reproductive success of the plant. As has been discussed above, the most common effect of heliotropism in flowers is the heating of reproductive structures, resulting in diverse advantages in terms of fitness. This is especially true in the case of diurnal heliotropism, and hence it is tempting to hypothesize that this phenomenon is more common at higher latitudes, where the ecological advantage on increasing flower temperature is likely to be more important. The graph in Fig. 5a shows the geographical distribution of the studies surveyed in this article. Most of the species reported to exhibit diurnal heliotropism belong to arctic and mountainous PT areas, while the plants studied in equatorial and tropical regions are mainly seasonally heliotropic (Fig. 5a). RI Nevertheless, among the species that show diurnal heliotropism there is no correlation between the relative heliotropic time (the proportion of the day that the flowers tracked the sun) and the latitude (Fig. SC 5b), and many of them occur in both mountainous and lowland habitats. U It is important to note that these geographically isolated observations do not represent all N habitats where the species exist, and there are some habitats that are under-represented. For instance A there must be a number of species also endemic to lowland regions or to countries of the southern M hemisphere, which have received less attention for scientific research. It is important to remark that although the studies cited above indicate that the main rewards of D heliotropism appear to be caused by consequent beneficial changes in irradiance and/or temperature, it TE remains elusive which processes or organs are responsible for increased fitness. Experimental studies are needed to investigate a possible association of the plant’s increase in reproductive success with the male CC EP or female reproductive parts, or other floral aspects. Furthermore, unraveling the relative importance of both irradiance and temperature for fitness as a consequence of heliotropism, warrants an in depth study. This may involve analyzing developmental regulation of reproductive organs and seeds, and production of A volatiles and a suitable physical flower environment for optimal interaction with pollinators, in a range of temperatures and irradiances. 6. CONCLUSIONS AND PERSPECTIVES Heliotropism of reproductive structures is a widespread response in the plant kingdom, and it is even present in fungi and algae. Despite the interesting advances on this topic, many questions that comprise different areas of knowledge (i.e. evolutionary, ecological up until the molecular scale) remain open. For example, from an evolutionary point of view we still ignore the phylogenetic origin of the PT heliotropic responses in the plant kingdom. We lack evidence of the existence of this phenomenon in RI reproductive structures and fruits in gymnosperms, and there is a shortage of information about the possibility of heliotropic responses in “primitive” angiosperm clades. Detailed characterization of this SC phenomenon in genera such as Amborella, Nuphur and Illicium, which are clades at the base of the U flowering plant lineage, could provide interesting insights into the evolutionary aspects of inflorescence N heliotropism of vascular plants. An additional question is whether seasonal and diurnal heliotropism share A similar origins, or if they arise from different evolutionary pathways. For this last subject, once the M mechanistic details are established, molecular studies might shed light on possible common signaling pathways of both responses. The availability of new molecular tools and next generation sequencing D techniques open new opportunities for advances in this area. TE In spite of the diversity of the heliotropic response of flowers and inflorescences and its occurrence in a wide variety of plant species and families, there is a common ecological significance: a positive impact CC EP on reproductive biology, in terms of size and/or quantity of seeds. Up until now, the benefits of heliotropism in reproductive organs have been mainly associated with the regulation of the temperature environment during fertilization / fruit development, and with positive effects on entomophillous A pollination. It is noteworthy that a temperature optimum for seed growth rate exists and deviations from this optimum strongly influence the yield of many crops such as wheat, common bean, soybean, sorghum, rice and barley (Chowdhury & Wardlaw 1978; Egli & Wardlaw 1980; Siddique & Goodwin 1980; Campbell et al. 1981; Kiniry & Musser 1988; Porter & Gawith 1999). In cold areas, the modification of the temperature of the inflorescence during seed maturation by the use of genetic lines with stronger heliotropic responses after pollination might mean an agronomical opportunity for the improvement of yield of crops. On the other hand, high temperatures can be harmful for flower development and seed production. For example, heliotropic flowers of plants native from cold areas (like Papaver species) may become damaged when grown in warm regions, especially when managed inside greenhouses where PT cooling systems are costly. In addition, high temperatures during the period of flowering reduce the RI success of fertilization and the seed growth rate (Egli & Wardlaw 1980; Ferris et al. 1998; Wheeler et al. 2000). In such conditions, the capacity to generate lines developing paraheliotropic or apheliotropic SC flowers (or leaves) may constitute an economical improvement. Furthermore, the process described by U Patiño et al. (2002) constitutes a unique case where a combination of heliotropism and floral morphology N (bell-shaped corollas of Convolvulaceae species) causes a cooling rather than a heating effect. This can A inspire alternative ways to generate a cooling solution to growing heliotropic flowers in warm TE ACKNOWLEDGEMENTS D M environments. We would like to thank the Ministry of Science, Technology and Productive Innovation (Argentina) CC EP and the FWO (Belgium) for providing a formal framework for the interaction of the groups that collaborated in the composition of this article. We acknowledge Dr. Hernán Boccalandro as an inspiration for our work on this topic. This work was supported by FWO project G000515N to F.V. and FWO-MINCYT A project VS00715N-FW/14/02 to D.V.D.S. and C.L.B. REFERENCES Allen D.K., Ohlrogge J.B. & Shachar‐Hill (2009) The role of light in soybean seed filling metabolism. The Plant Journal 58, 220–234. PT Asokanthan P.S., Johnson R.W., Griffith M. & Krol M. (1997) The photosynthetic potential of canola embryos. Physiologia Plantarum 101, 353–360. RI Atamian H.S., Creux N.M., Brown E.A., Garner A.G., Blackman B.K. & Harmer S.L. (2016) Circadian SC regulation of sunflower heliotropism, floral orientation, and pollinator visits. Science 353, 587–590. Bao L., Yamamoto K.T. & Fujita T. (2015) Phototropism in gametophytic shoots of the moss Physcomitrella N U patens. Plant Signaling & Behavior 10, e1010900. Bennett M.D, Smith J.B. & Kemble R. (1972) The effect of temperature on meiosis and pollen development A in wheat and rye. Canadian Journal of Genetics and Cytology, 14, 615-624. M Borghi M., Fernie A.R., Schiestl F.P. & Bouwmeester H.J. (2017) The sexual advantage of looking, smelling, and tasting good: the metabolic network that produces signals for pollinators. Trends in Plant Science TE D 22, 338–350. Campbell C.A., Davidson H.R. & Winkleman G.E. (1981) Effect of nitrogen, temperature, growth stage and CC EP duration of moisture stress on yield components and protein content of Manitou spring wheat. Canadian Journal of Plant Science 61, 549–563. Charles W.B., Harris R.E. (1972). Tomato fruit-set at high and low temperatures. Canadian Journal of Plant Science 52, 497-506. A Chittka L. & Raine N.E. (2006) Recognition of flowers by pollinators. Current Opinion in Plant Biology 9, 428–435. Chittka L., Shmida A., Troje N. & Menzel R. (1994) Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vision research 34, 1489–1508. Chowdhury S.I. & Wardlaw I.F. (1978) The effect of temperature on kernel development in cereals. Australian Journal of Agricultural Research 29, 205–223. Cooley J.R. (1995) Floral heat rewards and direct benefits to insect pollinators. Annals of the Entomological RI Corbet S.A. (1990) Pollination and the weather. Israel Journal of Botany 39, 13–20. PT Society of America 88, 576–579. Corbett A.L., Krannitz P.G. & Aarssen L.W. (1992) the influence of petals on reproductive success in the SC arctic poppy (Papaver radicatum). Canadian Journal of Botany 70, 200–204. U Córdova-Acosta E., Vite F. & Valverde P.L. (2012) Efecto de la orientación y caracteres de las flores en el N éxito reproductivo de Pachycereus weberi en la región de Tehuacán-Cuicatlán. Boletín de la Sociedad A Latinoamericana y del Caribe de Cactáceas y otras Suculentas 9, 7–8. M Darwin C. (1880) The power of movement in plants. D Delph L.F., Weinig C. & Sullivan K. (1998) Why fast-growing pollen tubes give rise to vigorous progeny: the TE test of a new mechanism. Proceedings of the Royal Society B: Biological Sciences 265, 935–939. Denisson D.S. (1965) Steady-state phototropism in Phycomyces. J Gen Physiol 48, 393–408. CC EP Egli D.B. & Wardlaw I.F. (1980) Temperature response of seed growth characteristics of soybeans. Agronomy Journal 72, 560–564. Ehleringer J. & Forseth I. (1980) Solar tracking by plants. Science 210, 1094–1098. A Ehleringer J., Mooney H.A., Gulmon S.L. & Rundel P. (1980) Orientation and its consequences for Copiapoa (Cactaceae) in the Atacama Desert. Oecologia 46, 63–67. Elgersma A., Stephenson A.G. & den Nijs A.P.M. (1989 ) Effects of genotype and temperature on pollen tube growth in perennial ryegrass (Lolium perenne L.). Sexual Plant Reproduction 2, 225-230. Farré-Armengol G., Iolanda F., Llusià J., Niinemets Ü. & Peñuelas J. (2014) Changes in floral bouquets from compound-specific responses to increasing temperatures. Global Change Biology 20, 3660–3669. Farré-Armengol G., Iolanda F., Llusià J., Niinemets Ü. & Peñuelas J. (2015) Optimum temperature for floral PT terpene emissions tracks the mean temperature of the flowering season. Functional Plant Biology 42, 851–857. RI Ferris R., Ellis R.H., Wheeler T.R. & Hadley P. (1998) Effect of high temperature stress at anthesis on grain SC yield and biomass of field-grown crops of wheat. Annals of Botany 82, 631–639. Galen C. (2006) Solar furnaces or swamp coolers: Costs and benefits of water use by solar-tracking flowers N U of the alpine snow buttercup, Ranunculus adoneus. Oecologia 148, 195–201. A Goffman F.D., Alonso A.P., Schwender J., Shachar-Hill Y. & Ohlrogge J.B. (2005) Light enables a very high M efficiency of carbon storage in developing embryos of rapeseed. Plant Physiology 138, 2269–2279. Griesbach R.J. (1987) Rhododendron flower color: Genetic/cultural interaction. Journal of the American D Rhododendron Society 41, 20–21. TE Griesbach R.J. (1992) Correlation of ph and light intensity on flower color in potted Eustoma grandiflorum CC EP Grise. HortScience 27, 817–818. Habermann G., Ellsworth P.F. V, Cazoto J.L., Feistler A.M., da Silva L., Donatti D.A. & Machado S.R. (2011) Leaf paraheliotropism in Styrax camporum confers increased light use efficiency and advantageous A photosynthetic responses rather than photoprotection. Environmental and Experimental Botany 71, 10–17. Halligan P. (1988) Light induced pigmentation patterning in Rhododendron corollas. Journal American Rhododendron Society 42. Hart J.W. (1990) Plant Tropisms: And other Growth Movements. Hedhly A., Hormaza J.I. & Herrero M. (2003) The effect of temperature on stigmatic receptivity in sweet cherry (Prunus avium) L. Plant, Cell and Environment 26, 1673– 1680. Herce M.F., Martorell C., Alonso-Fernandez C., Boullosa L.F.V. V & Meave J.A. (2013) Stem tilting in the radiation acquisition and temperature control. Plant Biology 16, 571–577. PT inter-tropical cactus Echinocactus platyacanthus: An adaptive solution to the trade-off between RI Hocking B. (1968) Insect-flower associations in the high arctic with special reference to nectar. Oikos 19, SC 359–387. Hohm T., Preuten T. & Fankhauser C. (2013) Phototropism: Translating light into directional growth. N U American Journal of Botany 100, 47–59. A Horth L., Campbell L. & Bray R. (2014) Wild bees preferentially visit Rudbeckia flower heads with M exaggerated Ultraviolet absorbing floral guides. Biology open 3, 221–230. Hu Z., Zhang H., Leng P., Zhao J., Wang W. & Wang S. (2013) The emission of floral scent from Lilium D “siberia” in response to light intensity and temperature. Acta Physiologiae Plantarum 35, 1691–1700. TE Iino M. (2001) Phototropism in higher plants. Comprehensive Series in Photosciences 1, 659–811. CC EP Jakobsen H.B. & Olsen C.E. (1994) Influence of climatic factors on emission of flower volatiles in situ. Planta 192, 365–371. Junghans T. & Fischer E. (2008) Aspects of dispersal in Cymbalaria muralis (Scrophulariaceae). Botanische A Jahrbücher 127, 289–298. Kagawa T., Kimura M. & Wada M. (2009) Blue light-induced phototropism of inflorescence stems and petioles is mediated by phototropin family members phot1 and phot2. Plant and Cell Physiology 50, 1774–1785. Kevan P. (1970) High arctic insect flower relations: the inter-relationships of arthropods and flowers at Lake Hazen, Ellesmere Island, N.W.T, Canada. Kevan P. (1972) Heliotropism in some arctic flowers. The Canadian field-naturalist 86, 41–44. PT Kevan P. (1975) Sun-tracking solar furnaces in high arctic flowers: significance for pollination and insects. RI Science 189, 723–726. Kevan P.G. (1973) Flowers, insects, and pollination ecology in the canadian high Arctic. Polar Record 16, SC 667–674. U Kiendl H. (1940) Über die auslosung von postflorationserscheinungen durch β-indolyllessigsaure. Planta N 31, 230–243. M grain filling. Agronomy journal 80, 606–610. A Kiniry J.R. & Musser R.L. (1988) Response of kernel weight of sorghum to environment early and late in D Kjellberg B., Karlsson S. & Kerstensson I. (1982) Effects of heliotropic movements of flowers of Dryas TE octopetala L. on gynoecium temperature and seed development. Oecologia 54, 10–13. Knutson R.M. (1981) Flowers that make heat while the sun shines. Natural History 90, 75–80. CC EP Koller D. (1986) The control of leaf orientation by light. Photochemistry and Photobiology 44, 819–826. Koller D. (2011) The Restless Plant. A Koski M.H. & Ashman T.L. (2014) Dissecting pollinator responses to a ubiquitous ultraviolet floral pattern in the wild. Functional ecology 28, 868–877. Krannitz P.G. (1996) Reproductive ecology of Dryas integrifolia in the high arctic semi-desert. Canadian Journal of Botany 74, 1451–1460. Kudo G. (1995) Ecological significance of flower heliotropism in the spring ephemera Adonis ramosa (Ranunculaceae). 72, 14–20. Kumar P. & Kiss J.Z. (2006) Modulation of phototropism by phytochrome E and attenuation of gravitropism PT by phytochromes B and E in inflorescence stems. Physiologia Plantarum 127, 304–311. Kumar P., Millar K.D.L. & Kiss J.Z. (2011) Inflorescence stems of the mdr1 mutant display altered RI gravitropism and phototropism. Environmental and Experimental Botany 70, 244–250. U in Arabidopsis thaliana. Functional Plant Biology 35, 298–305. SC Kumar P., Montgomery C.E. & Kiss J.Z. (2008) The role of phytochrome C in gravitropism and phototropism N Kutschera U. & Briggs W.R. (2016) Phototropic solar tracking in sunflower plants: an integrative A perspective. Annals of Botany 117, 1–8. M Lang A.R.. & Begg J.. (1979) Movements of Helianthus annuus leaves and heads. 16, 299–305. TE Botany 103, 1159–1163. D Li J.K. & Huang S.Q. (2009) Flower thermoregulation facilitates fertilization in asian sacred lotus. Annals of Luzar N. & Gottsberger G. (2001) Flower heliotropism and floral heating of five alpine plant species and CC EP the effect on flower visiting in Ranunculus montanus in the Austrian Alps. Arctic, Antarctic, and Alpine Research 33, 93–99. Millar A.J. (2003) A suite of photoreceptors entrains the plant circadian clock. Journal of biological rhythms A 18, 217–226. Mølgaard P. (1989) Temperature relations of yellow and white flowered Papaver radicatum in North Greenland. Arctic and Alpine Research 21, 83–90. Niinemets Ü., Loreto F. & Reichstein M. (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends in plant science 9, 180–186. Nobel P.S. (1981) Influences of photosynthetically active radiation on cladode orientation, stem tilting, and height of cacti. Ecology 6, 982–990. Noh B., Murphy A.S. & Spalding E.P. (2001) Multidrug resistance–like genes of Arabidopsis required for PT auxin transport and auxin-mediated development. The Plant Cell 13, 2441–2454. Oehlkers F. (1922) Die postfloralen Krümmungen des Blütenstieles von Tropaeolum majus und das RI Problem der Umstimmung. Jahrbücher für wissenschaftliche Botanik 61, 66–125. SC Orueta D. (2002) Thermal relationships between Calendula arvensis inflorescences and Usia aurata U bombyliid flies. Ecology. 83, 3073-3085. N Patiño S., Jeffree C. & Grace J. (2002) The ecological role of orientation in tropical convolvulaceous flowers. A Oecologia 130, 373–379. M Pedmale U. V., Celaya R.B. & Liscum E. (2010) Phototropism: Mechanism and Outcomes. The Arabidopsis D Book 8, e0125. Peet M.M., Sato S. & GardnerR.G (2002) Comparing heat stress effects on male-fertile and male-sterile TE tomatoes. Plant, Cell and Environment 21, 225–231. CC EP Petanidou T. & Smets E. (1996) Does temperature stress induce nectar secretion in mediterranean plants ? New Phytologist 133, 513–518. Peterson M.L., Miller T.J. & Kay K.M. (2015) An ultraviolet floral polymorphism associated with life history A drives pollinator discrimination in Mimulus guttatus. American journal of botany 102, 396–406. Pigott C.D. & Huntley J.P. (1981) Factors controlling the distribution of Tilia cordata at its northern limit of its geographical limits. III. Nature and Causes of Seed Sterility. New Phytologist 87, 817–839. Porter J.R. & Gawith M. (1999) Temperatures and the growth and development of wheat: a review. Temperatures and the growth and development of wheat: a review. 10, 23–26. Rejšková A., Brom J., Pokorný J. & Korečko J. (2010) Temperature distribution in light-coloured flowers and inflorescences of early spring temperate species measured by Infrared camera. Flora-Morphology, Distribution, Functional Ecology of Plants 205, 282–289. PT Ross J.J., O’Neill D.P. & Rathbone D.A. (2003) Auxin-gibberellin interactions in pea: integrating the old with the new. Journal of Plant Growth Regulation 22, 99–108. SC II efficiency. Environmental and experimental botany 36, 431–438. RI Sailaja M. V. & Rama Das V. (1996) Leaf solar tracking response exhibits diurnal constancy in photosystem Sato A., Sasaki S., Matsuzaki J. & Yamamoto K.T. (2014) Light-dependent gravitropism and negative U phototropism of inflorescence stems in a dominant Aux/IAA mutant of Arabidopsis thaliana, axr2. A N Journal of plant research 127, 627–639. M Scace P.D. (2001) The Floral Artist's Guide: A Reference to Cut Flowers and Foliages. Cengage Learning, Boston (MA). D Schlangen K., Miosic S., Castro A., Freudmann K., Luczkiewicz M., Vitzthum F., … Halbwirth H. (2009) TE Formation of UV-honey guides in Rudbeckia hirta. Phytochemistry 70, 889–898. CC EP Schmitt M.E. (1922) Beziehun gen zwischen der Befruchtung und den postfloralen Blüten- bzw. Fruchtstielb ewegungen bei Digitalis purpurea, Digitalis ambigua, Althaea rosea und Linaria cymbalaria. Zeitschrift botanische 14, 625–675. A Sherry R.A. & Galen C. (1998) The mechanism of floral heliotropism in the snow buttercup, Ranunculus adoneus. Plant, Cell and Environment 21, 983–993. Siddique M.A. & Goodwin P.B. (1980) Seed vigor in bean (Phaseolus vulgaris L. cv. Apollo) as influenced by temperature and water regime during development and maturation. Journal of Experimental Botany 31, 313–323. Smith A.P. (1975) Insect pollination and heliotropism in Oritrophium limnophilum (Compositae) of the Andean Páramo. Biotropica 7, 284–286. Spaethe J., Tautz J. & Chittka L. (2001) Visual constraints in foraging bumblebees: flower size and color PT affect search time and flight behavior. Proceedings of the National Academy of Sciences 98, 3898– 3903. RI Stanton M.. & Galen C. (1993) Blue light controls solar tracking by flowers of an alpine plant. Plant, Cell SC and Environment 16, 983–989. Stanton M.L. & Galen C. (1989) Consequences of flower heliotropism for reproduction in an alpine N U buttercup (Ranunculus adoneus). Oecologia 78, 477–485. A Steere W.C. (1973) Observations on the Genus Aplodon (Musci: Splachnaceae). The Bryologist 76, 347– M 335. Stephenson A., Lau T., Quesada M. & Winsor J.A. (1992) Factors that affect pollen performance. In: Wyatt D R. ed. Ecology and evolution of plant reproduction: new approaches., 119– 136. TE Takahashi M. & Mikami K. (2016) Phototropism in the arine Red Macroalga Pyropia yezoensis. American CC EP Journal of Plant Sciences 7, 2412–2428. Thanisawanyangkura S., Sinoquet H., Rivet P., Cretenet M. & Jallas E. (1997) Leaf orientation and sunlit leaf area distribution in cotton. Agricultural and Forest Meteorology 86, 1–15. A Thomas R.J., Caron P.J. & Rebecca S. Watt (1987) Time-lapse photography of phototropism in Pellia epiphylla. The Bryologist 90, 390–392. Totland O. (1996) Flower heliotropism in an alpine population of Ranunculus acris (Ranunculaceae): Effects on flower temperature, insect visitation, and seed production. American Journal of Botany 83, 452– 458. Vandenbrink J.P., Brown E.A., Harmer S.L. & Blackman B.K. (2014) Turning heads: The biology of solar tracking in sunflower. Plant Science 224, 20–26. Vandenbussche F., Tilbrook K., Fierro A.C., Marchal K., Poelman D., Van Der Straeten D. & Ulm R. (2014) PT Photoreceptor-mediated bending towards UV-B in Arabidopsis. Molecular Plant 7, 1041–1052. Wada N. (1998) Sun-tracking flower movement and seed production of mountain avens, Dryas octopetala RI L. in the high arctic, ny-alesund, svalbard. Proceedings of the NIPR Symposium on Polar Biology11, SC 128-136. Wang H., Xiao C.-L., Gituru R.W., Xiong Z., Yu D., Guo Y.-H. & Yang C.-F. (2014) Change of floral orientation U affects pollinator diversity and their relative importance in an alpine plant with generalized A N pollination system, Geranium refractum (Geraniaceae). Plant Ecology 215, 1211–1219. Warren S.D., Baggett L.S. & Warren H. (2016) Directional Floral Orientation in Joshua Trees (Yucca M brevifolia). Western North American Naturalist 76, 374–378. Weston D.E., Reid J.B. & Ross J.J. (2009) Auxin regulation of gibberellin biosynthesis in the roots of pea TE D (Pisum sativum). Functional Plant Biology 36, 362–369. Wheeler T.R., Craufurd P.Q., Ellis R.H., Porter J.R. & Prasad P. V. (2000) Temperature variability and the CC EP yield of annual crops. Agriculture, Ecosystems & Environment 82, 159–167. Whippo C.W. & Hangarter R.P. (2006) Phototropism: bending towards enlightenment. The Plant Cell 18, 1110–1119. A Willige B.C., Isono E., Richter R., Zourelidou M. & Schwechheimer C. (2011) Gibberellin regulates PINFORMED abundance and is required for auxin transport–dependent growth and development in Arabidopsis thaliana. The Plant Cell 23, 2184–2195. Wilson P. (1994) The east-facing flowers of Drosera tracyi. American Midland Naturalist 131, 366–369. Yoshioka Y., Horisaki A., Kobayashi K., Niikura S., Ninomiya S. & Ohsawa R. (2005) Intraspecific variation in the ultraviolet colour proportion of flowers in Brassica rapa L. Plant breeding 124, 551–556. Young T.P. (1984) Solar irradiation increases floral development rates in afro-alpine Lobelia telekii. PT Biotropica 16, 243–245. Zavala-Hurtado J.A., Vite F. & Ezcurra E. (1998) Stem tilting and pseudocephalium orientation in RI Cephalocereus columna-trajani (Cactaceae): A functional interpretation. Ecology 79, 340–348. SC Zhang S., Ai H.L., Yu W. Bin, Wang H. & Li D.Z. (2010) Flower heliotropism of Anemone rivularis (Ranunculaceae) in the Himalayas: Effects on floral temperature and reproductive fitness. Plant N U Ecology 209, 301–312. A Zhao D., Tao J., Han C. & Ge J. (2012) Flower color diversity revealed by differential expression of flavonoid M biosynthetic genes and flavonoid accumulation in herbaceous peony (Paeonia lactiflora Pall.). Molecular biology reports 39, 11263–11275. D Zhao D., Tao J., (2015) Recent advances on the development and regulation of flower color in ornamental TE plants. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2015.00261. CC EP Zinsmeister H.D. (1960) Das phototropische Verhalten der Blütenstiele von Cyclamen persicum Hybr. A Handbook of flowering 55, 647–668. Figure 1: (a)-(d) Examples of flowers oriented toward the sun in and around Merelbeke and Oosterzele (Belgium). (a) Alliaria petiolata, (b) taraxacum officinale, (c) Ranunculus acris, (d) Cardamine hirsuta and Arabidopsis thaliana. (e) Inflorescences of Centranthus ruber oriented toward the sun in the Ghent PT University Botanical Garden. RI Figure 2: Description of the different flower movements adopted as a measure of heliotropic response by different authors: (a) the horizontal component of the angle between the flower and the sun, measured SC on a plane perpendicular to gravity vector (Kevan 1972; Luzar & Gottsberger 2001) (b) the vertical U component of the angle between the flower and the sun, measured on a plane perpendicular to the Earth N surface (Stanton & Galen 1989, Zhang et al. 2010). (c) a tridimensional combination of both angles (Stanton A & Galen 1989, Totland 1996, Zhang et al. 2010). (d) the compass orientation (on a plane perpendicular to M gravity vector) relative to the east. (e) the elevation angle (vertical) incorporating an east/west discrimination. The short spaced dotted arrow indicates direction of projection against an east-west TE D oriented plane (Lang and Begg 1979, Vandenbrink et al. 2014). Figure 3. Heliotropic responses (in terms of horizontal deviation from the sun) of seven species for which CC EP quantitative data is available in literature, contrasting their behavior with ideal plants (orange dash-lines) showing perfect seasonal or daily heliotropism in arctic (a), alpine (b) and equatorial (c) regions according to the place where the measurements were taken. It is noteworthy that only Papaver radicatum (a) and A Ranunculus montanus (b) show diurnal heliotropism. Figure 4. Mechanisms described for model systems of (a) diurnal and (b) potential seasonal heliotropic responses. On each panel, green arrows indicate promotion; red truncated arrows indicate repression; double head arrows indicate growth; purple gradients represent auxin concentration gradients; “IAA” = Indole 3-acetic acid (auxin); “GAs” = Gibberellin. (a) Example of diurnal heliotropism: Helianthus annuus. Heliotropic movements of sunflower heads result from auxin-driven differential growth between east and west sides of the inflorescence stem, in response to blue light stimuli. The periodicity of diurnal heliotropism is controlled by the circadian clock, which regulates the differential expression of auxin- PT inducible genes between both sides of the stem and consequently the changes in auxin gradients from day RI to night. Moreover, stem growth promoted by gibberellins is essential for the heliotropic movement (Atamian et al. 2016). (b) Example of potential seasonal heliotropism: Arabidopsis thaliana. UV-B signaled SC by the UVR8 photoreceptor and blue light perceived by phototropins promote positive phototropism U (Liscum & Briggs 1995, Kagawa et al., 2009, Vandenbussche et al., 2014), a response that is negatively N regulated by phyC and phyD (Kumar et al., 2008). In the special case of inflorescence, phyE has a positive A effect (Kumar & Kiss 2006), in consonance with phototropins. The curvature results from a differentiality M between the growth rates of illuminated and shaded tissues, generated by an auxin gradient established upon unilateral blue light exposure. The redistribution of a basal (locally pre-existing) amount of the D hormone is sufficient to induce the phototropic movement. However, higher amounts of auxins imported TE from the apex (the main source of the hormone) by auxin transporters such as ABCB19 do not appear to account for this response (Christie et al. 2011, Kumar et al., 2011). Conversely, inadequate distribution or CC EP too little auxin signaling results in no or even negative phototropism. Figure 5. (a) Geographic distribution of the reported cases of diurnal and seasonal heliotropism. (b) A Relation between the heliotropic time (the proportion of the day during which the flower tracks the sun) and the latitude where the study was performed. A Pearson's product-moment correlation test was carried out yielding no significant correlation between variables (Pearson's coefficient r=0.23). The p-value yielded by a linear regression analysis is 0.479, indicating no effect of latitude on heliotropic time. CC EP A D TE PT RI SC U N A M Figure 1. CC EP A D TE PT RI SC U N A M Figure 2 CC EP A D TE PT RI SC U N A M Figure 3 CC EP A D TE PT RI SC U N A M Figure 4 CC EP A D TE PT RI SC U N A M Figure 5 CC EP A D TE PT RI SC U N A M Box 1. Glossary Heliotropism: any type of process that modifies an organ orientation in response to the sun position (Kevan 1972; Ehleringer et al. 1980; Koller 1986; Hart 1990; Stanton & Galen 1993; Thanisawanyangkura et al. 1997) Orthoheliotropism: those cases of heliotropism in which the organ orients orthogonally to the sun rays. PT http://www.encyclo.co.uk (May, 2017) Apheliotropism: those cases of heliotropism in which the organ bends away from the sun rays Darwin (1880) RI Paraheliotropism: those cases of heliotropism in which the organ orients parallel to the sun rays. (Ehleringer et al. 1980; Koller 1986; Thanisawanyangkura et al. 1997; Habermann et al 2011) SC Diaheliotropism: those cases of heliotropism in which the organ orients perpendicular to the sun rays. (Ehleringer et al. 1980; Koller 1986; Thanisawanyangkura et al. 1997; Habermann et al 2011) U Diurnal Heliotropism: when the adjustment of the orientation of the heliotropic organ occurs in periods of about 24 h. (Defined in the present article) N Seasonal Heliotropism: when the response happens only once and the orientation acquired by the organ remain essentially constant. A (Patiño et al. 2002) M Horizontal Heliotropism: when plant tracks the compass (or azimuthal) orientation of the sun (along the horizontal plane) (Defined in the present article) Vertical Heliotropism: when plant tracks the variation of the sun elevation from the horizon (along the vertical plane). A CC EP TE D (Defined in the present article)