Plant niche construction for available nutrients, water, light, and oxygen

Although plants (unlike motile microorganisms and foraging animals) lack the option of moving to resource-rich locations, they do have an impressive developmental repertoire that can serve to enhance their experience of the below- and above-ground resource conditions they encounter as sessile organisms (Huey et al. 2002). The concentration of essential plant nutrients varies widely in soils of natural habitats at within- and among-individual scales, both spatially and temporally (Bazzaz 1996; Hodge 2010; and references therein). Individual plants are able to experience an environment that is consistently high in nutrients despite this resource patchiness because of the developmental and physiological plasticity of root systems. This resource enhancement is accomplished through the following specific changes to plant "foraging behavior" (sensu M. Hutchings and de Kroon 1994): (a) adjustments in total surface area of root systems in response to soil nutrient levels; (b) targeted proliferation of new roots in nutrient-rich locations; and (c) increased systemic rates of mineral ion uptake in those locations (Hodge 2009 and references therein).

One well-studied developmental response to nutrient-poor soil is increased biomass allocation to root tissue relative to shoots (Fitter and Hay 2002). This allocational adjustment is often accompanied by a morphological shift to thinner roots that have a higher surface-to-volume ratio (Fitter 1994; Bell and Sultan 1999; and references therein). Together, these responses result in a much greater root-system length and surface area per gram of tissue to be supplied, allowing the plant to take in more mineral ions from its rhizosphere and hence experience it as a less nutrient-poor environment (Sultan and Bazzaz 1993c).

Plastic, targeted root proliferation was first investigated in a series of classic lab experiments during the 1970s (e.g., Drew et al. 1973; further references in Hodge 2004). In these studies, individual barley plants, Hordeum vulgare, were grown in containers that were divided into compartments containing different concentrations of a given macronutrient (nitrate, ammonium, potassium, or phosphate). Plants grown in containers that had a high concentration of the nutrient in all three compartments showed consistent root proliferation throughout the container. In contrast, individuals grown in containers with two low-nutrient compartments and a single, very high-nutrient compartment showed intense proliferation of lateral roots in this nutrient- rich zone, and very little lateral root production in the nutrient-poor compartments (Drew 1975; confirmed in several species by Robinson 1994). Localized proliferation based on relative resource richness reflects the number of new primary and especially lateral roots initiated, as well as the elongation and further branching of these fine, physiologically active roots (Hodge 2009). The proliferation response, which is highly dynamic, is apparently governed by a combination of local sensors (which recognize the immediate concentration of soil resources) and systemic signals (which reflect the plant's previous resource acquisition); even in the presence of very high nitrate levels, for instance, the response occurs only when the plant is nutrient stressed (de Kroon et al. 2009 and references therein).

The physiological component of plant nutrientforaging plasticity is equally dramatic: in most species, roots of nutrient-deprived plants transiently increase uptake rates for mineral ions from 2-fold to 11-fold in response to a local increase in nutrient supply (Hodge 2004). This short-term increase in nutrient uptake may provide an internal signal for the plant to initiate new root investment at this nutrient-rich location.

Two other key soil resources for plants are water and oxygen. Individuals express the same kind of foraging adjustments to enhance the availability of these resources: increased whole-plant allocation to root tissues in dry soil or to oxygen-collecting organs such as pneumatophores in flooded conditions; rapid, targeted root proliferation in moist or aerated soil locations in the event of water or oxygen stress; and changes to uptake thresholds and utilization (conductance or respiration) rates (references in Bell and Sultan 1999; Fitter and Hay 2002; Sultan 2003).

Developmental and physiological plasticity also allow plants to experience favorable levels of aboveground resources such as light, oxygen, and carbon dioxide. In low-light conditions, plants maximize the total surface area for catching photons through increased leaf biomass allocation and morphological changes to leaves (Chapter 2, Section 2.3.4; Ryser and Eek 2000; Fitter and Hay 2002). "Shade" leaves produced in low light are anatomically altered so as to most efficiently utilize a less dense photon flux (i.e., with a single layer of chloroplast-rich palisade parenchyma; references in Sultan 2003). Access to solar radiation at the whole-plant level is also determined by crown architecture, that is, by the deployment of individual leaves and branches in space (reviewed by M. Hutchings and de Kroon 1994; Valladares and Ninimets 2007). Within phyloge- netically constrained parameters, plants adjust leaf angle and placement through developmental shifts in internode and petiole length, as well as through diurnal movements (Fleck et al. 2003; Huber et al. 2008). For example, leaves may be held more vertically in the upper part of an individual's canopy, and more horizontally at lower levels, allowing more light to penetrate to the latter and hence maximizing whole-plant insolation (Valladares and Ninimets 2007). The production of broad, thin "shade leaves" lower in the canopy helps to maximize light interception as well. Increased production of vegetative buds on branches in high-light positions can also result in effective light foraging, analogous to root proliferation in resource-rich soil patches. Because the exposure of shoot organs to direct sun also influences the temperature of leaf tissues and their water status, these adjustments simultaneously shape several aspects of the plant's experienced environment (Valladares and Pearcy 1997; Valladares and Ninimets 2007). For example, leaf- and branch-level adjustments can also allow a plant to avoid the negative effects of photoinhibition and heat stress in conditions of high insolation and moisture deficit (Valladares and Pearcy 1997).

Several fascinating aspects of plant experiential niche construction take place within the leaves, where the supply of photosynthetically active radiation is shaped by dynamic ultrastructural adjustments. One such adjustment consists of orientation movements that redistribute chloroplasts within leaf mesophyll cells, first described in 1908 (reviewed by Wada et al. 2003). These light-processing organelles move continuously inside cells, in response to the flux density, direction, and spectral quality of light (Haupt and Scheuerlein 1990; W. Williams et al. 2003). In weak light, chloroplasts accumulate across cell surfaces that are perpendicular to the direction of incident light, maximizing the cell's photon harvest (Kasahara et al. 2004; Davis and Hangarter 2012). By contrast, under strong ir- radiance, chloroplasts line up along the side walls of the cell, parallel to the angle of light (Figure 4.5a). This chloroplast "avoidance" response allows more light to be transmitted through the leaf tissue, protecting the photosynthetic machinery of the cell from photodamage due to excess energy (Kasahara et al. 2002; Gabrys 2012). Oddly enough, it also makes it possible to create images within living leaf tissues, by "drawing" with direct irradiance (Figure 4.5b). Although their regulatory mechanisms are not yet fully understood (Wada et al. 2003; Davis and Hangarter 2012), these niche-constructing intracellular movements, and the phototropin blue- light receptors that mediate them, are evidently conserved across algae, mosses, ferns, and angio- sperms (references in DeBlasio et al. 2003).

At an even finer level, plants modulate their experienced light environment by means of plastic ultrastructural changes to photon-processing components of chloroplasts themselves (Kirchhoff 2013). In Arabidopsis, for instance, plants grown in low light alter the morphology and conformation of thylakoid membranes and structurally rearrange Photosystem II protein supercomplexes, so as to more efficiently transfer energy between photosystems (Kouril et al. 2013). Analogous ultrastructural changes take place in a distantly related photosynthetic organism, the purple bacterium Rhodopseudomonas palustris: in this proteobacterium, the number, protein composition, and size of lightharvesting units change in response to contrasting light levels, resulting in changed cellular light absorbance spectra (Brotosudarmo et al. 2011). It appears that plants, algae, and photosynthetic bacteria may shape their experienced light environment even at the atomic level, by means of a biophysical mode of plasticity known as quantum coherence (discussed by Anna et al. 2014). Through coherence, a photon-excited electron within a chlorophyll molecule interacts with its protein scaffold so as to realize a wave-like transfer of energy that moves across the light-harvesting system, unerringly finding the most efficient path (Engel et al. 2007). It is believed that quantum coherence could explain the remarkable, near-perfect efficiency at which solar energy is captured for conversion to chemical energy during photosynthesis, a biophysical behavior that maximizes the availability of light as a resource.

Developmental responses at several levels also allow plants to experience an enhanced oxygen environment in the event of flooding. Plants of flood-prone habitats confront a severe drop in atmospheric oxygen if shoots become submerged. Individuals respond to this challenge with species-specific morphological and ultrastructural changes that allow them to experience the environment as one with sufficient oxygen. In some taxa, submerged shoots produce leaves with enlarged surface area, thinner cuticles, and thinner epidermal cell walls, changes that jointly enhance the plant's internal supply of carbon dioxide (Mommer et al. 2005). Together with a reorientation of chloro- plasts toward the epidermis, these changes lead to higher underwater photosynthetic rates that result in elevated tissue oxygen concentration despite the poor solubility and diffusion of oxygen in water (Mommer and Visser 2005; Mommer et al. 2006). In other species, stems or petioles on submerged shoots rapidly elongate, or orient more vertically, so that leaves maintain direct contact with the oxygen- rich aerial environment (Voesenek et al. 2006 and references therein). One signal for this elongation response is an internal one, the buildup of the gaseous hormone ethylene due to reduced gas diffusion out of plant tissues under water (Bailey-Serres and Voesenek 2010). Interestingly, subsequent to the initiating cues (ethylene rather than phytochrome signals), elongation responses to flooding and shade-avoidance shoot responses are mediated by largely shared hormonal pathways (Sultan 2010 and references therein). Physiological shifts to alternative metabolic pathways can also help plants to avoid experiencing an oxygen deficit (Bailey-Serres and Voesenek 2010). Response to flooding is one of the few cases in which species differences in ecological developmental response capacities have

Chloroplast movements within plant cells mediate the supply and intensity of photosynthetically active radiation

Figure 4.5 Chloroplast movements within plant cells mediate the supply and intensity of photosynthetically active radiation.

(a) In darkness (I) or weak light (II), chloroplasts cover cell surfaces, maximizing photon interception; in strong light (III), they move to cell margins, thus allowing solar energy to pass through the cell. Image courtesy of Mark Fricker. For the color image, see plate 13. (b) Because light-induced chloroplast movements alter light transmission, they can be used to reproduce a high-contrast image (such as a photograph) within leaf tissue. After approximately 45 minutes of blue-light illumination, the areas where light reached the leaf will be more transparent than those covered by dark parts of the image. A portrait of the pioneering plant physiologist Julius von Sachs is here reproduced in a live coleus leaf. In his 1887 Lectures on the physiology of plants, Sachs was the first to observe that a "light-picture" could be created in living leaf tissue. leaf portrait courtesy of Roger Hangarter. For the color image, see Plate 14.

been studied both mechanistically and with respect to realized ecological consequences in the field (Vo- esenek et al. 2004; Benschop et al. 2005).

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