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A Latitudinal Cline and Response to Vernalization in Leaf

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A Latitudinal Cline and Response to Vernalization in Leaf Research ABlackwell Publishing latitudinalLtd cline and response to vernalization in leaf angle and morphology in Arabidopsis thaliana (Brassicaceae) Robin Hopkins1,2, Johanna Schmitt1 and John R. Stinchcombe3 1Ecology and Evolutionary Biology, Brown University, Providence, RI, USA; 2Present address: Biology, Duke University, Durham, NC, USA; 3Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S 3B2, Canada Summary Author for correspondence: • Adaptation to latitudinal patterns of environmental variation is predicted to result Robin Hopkins in clinal variation in leaf traits. Therefore, this study tested for geographic differen- + Tel: 1 (919) 660 7223 tiation and plastic responses to vernalization in leaf angle and leaf morphology in Fax: +1 (919) 660 7293 Email: [email protected] Arabidopsis thaliana. • Twenty-one European ecotypes were grown in a common growth chamber envi- Received: 14 November 2007 ronment. Replicates of each ecotype were exposed to one of four treatments: 0, 10, Accepted: 25 February 2008 20 or 30 d of vernalization. • Ecotypes from lower latitudes had more erect leaves, as predicted from functional arguments about selection to maximize photosynthesis. Lower-latitude ecotypes also had more elongated petioles as predicted by a biomechanical constraint hypoth- esis. In addition, extended vernalization resulted in shorter and more erect leaves. • As predicted by functional and adaptive hypotheses, our results show genetically based clinal variation as well as environmentally induced variation in leaf traits. Key words: Arabidopsis thaliana, latitudinal cline, leaf angle, leaf morphology, population differentiation, vernalization. New Phytologist (2008) 179: 155–164 © The Authors (2008). Journal compilation © New Phytologist (2008) doi: 10.1111/j.1469-8137.2008.02447.x more subtle environmental variation can also result in Introduction morphological adaptations to maximize photosynthesis while Clinal variation in ecologically important traits is considered minimizing transpiration. to be strong evidence of adaptation to geographically varying Leaf characteristics play a critical role in determining rates selection (Mayr, 1956; Endler, 1977; Caicedo et al., 2004; of photosynthesis and transpiration (Baldocchi et al., 1985; Stinchcombe et al., 2004; Stillwell et al., 2007). Sessile Niklas, 1993; Smith & Whitelam, 1997). Leaf angle, the angle organisms, such as plants, can experience considerable a leaf deviates from horizontal to ground, directly affects the variation in natural selection across their range, and local flux of solar energy per unit leaf area, and is thus an important adaptation to such selection can result in geographic factor in determining the maximum photosynthetic ability differentiation of populations (Joshi et al., 2001; Streisfeld & of a plant (Ehleringer, 1988; Ridao et al., 1996; Falster & Kohn, 2005; Springer, 2007). Traits in leaves, the organs of Westoby, 2003). Photosynthesis models predict that optimal photosynthesis and transpiration, are likely to experience leaf angle at lower latitudes is more erect than optimal leaf clinal variation in selection as a result of latitudinal differences angle at higher latitudes (Baldocchi et al., 1985; Ehleringer, in day length, light intensity, solar angle, and temperature. 1988; Herbert, 2003). Because the standard photosynthetic One of the primary physiological constraints on plants is light response curve saturates at moderate light intensities, the need to maximize photosynthesis and minimize water plants at low latitudes can actually maximize photosynthesis loss. Extreme environments, such as deserts, have resulted in in the intensity of midday sun, and decrease water loss and the extreme morphological adaptations, such as cactus spines, but deleterious effects of high leaf temperatures, by increasing leaf www.newphytologist.org 155 156 Research angle and avoiding direct vertical light on the leaf blade Temperature is one important environmental regulator of (Bjorkman & Powles, 1984; Ehleringer, 1988; Ridao et al., plant growth and development that varies across a latitudinal 1996; Smith et al., 1998; Falster & Westoby, 2003). In addi- gradient. There are two important aspects of temperature: tion, more vertical leaves have greater photosynthetic ability at ambient temperature, the average temperature at which a the beginning and end of the day when the sun is at shallower plant undergoes most of its growth and reproduction, and angles. Greater leaf angles decrease transpiration and heat vernalization, which refers to an extended period of cold. damage by decreasing direct exposure to high-intensity Studies have demonstrated a strong effect of ambient temper- light (Bjorkman & Powles, 1984; Ehleringer, 1988; Ridao ature on vegetative growth (Weinig, 2000; Heggie & Halliday, et al., 1996). 2005). In particular, warmer temperatures have been shown Functional studies, which predict that greater leaf angle in to result in increased auxin production and thus hypocotyl lower latitudes maximizes photosynthesis and decreases water elongation (Gray et al., 1998). In addition, genetic pathways loss, provide an adaptive explanation for observed latitudinal that have been shown to affect leaf morphology interact trends in leaf angle (McMillen & McClendon, 1979; Ehleringer, intricately with temperature-sensing pathways (Mazzella 1988; Halloy & Mark, 1996; Ridao et al., 1996; Werner et al., 2000; Halliday et al., 2003; Halliday & Whitelam, et al., 1999; Barclay, 2001; Falster & Westoby, 2003; Kalapos 2003). Vernalization, or prolonged exposure to cold temper- & Csontos, 2003). Two field studies, focusing mostly on atures, has been shown to be necessary for the transition trees, have detected steeper leaf angles and smaller leaf surfaces between vegetative and reproductive growth for some plants in communities with either lower levels of precipitation or (Bastow et al., 2004; Amasino, 2005; Trevaskis et al., 2007), higher levels of available light (Ehleringer, 1988; Smith et al., but, to date, there has been very little direct investigation of 1998). Studies of a single species across its range have also how vernalization, or over-wintering, affects leaf morphology found latitudinal clines in leaf angle (Ezcurra et al., 1991; (for an exception see Lee & Amasino, 1995). Studying how Herbert, 1991, 2003). However, all of these studies were plant vegetative tissue (i.e. leaf angle and leaf length) conducted by measuring traits on plants growing in the field, responds to variation in vernalization may provide a more and therefore did not test whether the observed clines are a complete understanding of how plants may have adapted to result of genetic differentiation, or environmentally induced variation in environmental conditions across a range of plastic responses to geographic differences in growing conditions. latitudes. In contrast to the predictions about leaf angle variation, Here we test for latitudinal differentiation and the effect of there are more complex hypotheses about how environmental vernalization in leaf angle and morphology in 21 European variation influences selection on other aspects of leaf mor- genotypes of the model species Arabidopsis thaliana grown phology. Previous studies have found that, in general, leaf size under common controlled environmental conditions. Arabi- can increase with increasing average temperature (McDonald dopsis thaliana grows in a wide variety of climates across its et al., 2003; Thuiller et al., 2004). Large leaves have thicker native range (Hoffmann, 2002), and phenotypic clines sug- boundary layers of air around their surfaces which insulate gestive of adaptive differentiation have recently been observed and decrease water loss through transpiration (Parkhurst & in several ecologically important traits (Li et al., 1998; Maloof Loucks, 1972; Schuepp, 1993; Westoby et al., 2002). Fur- et al., 2001; Stenoien et al., 2002; Stinchcombe et al., 2004; thermore, leaves from moister environments tend to be Lempe et al., 2005). To date there have been no reports of larger than leaves from drier climates (Parkhurst & Loucks, clinal genetic differentiation in leaf angle in A. thaliana or other 1972; Schuepp, 1993; Thuiller et al., 2004). Thus, temper- species. We also investigated two aspects of leaf morphology: ature and moisture gradients across latitudinal transects may leaf length, a general measure of leaf size, and leaf ratio, the inform hypotheses about large-scale geographic variation in ratio of leaf blade length to total leaf length. Specifically, we leaf traits. Alternatively, variation in leaf traits tends to be asked the following questions. correlated, and thus a change in leaf size or morphology • Do ecotypes show variation in leaf angle and leaf mor- could be a result of a correlated effect of change in leaf angle. phology across a latitudinal gradient as predicted by func- As leaf angle increases, the force required to hold up a leaf tional arguments? blade decreases and thus plants in lower latitudes may • Does the duration of vernalization affect leaf morphology have elongated leaves because of a release from a biomechan- and leaf angle? ical constraint (Niklas, 1999). To date, there have been few surveys of within-species variation in leaf morphology across Materials and Methods a very large geographic range, and thus there is a need for further empirical evidence to elucidate the important factors Study organism affecting leaf size. Variation in both leaf angle and
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