Cue and response systems: plant and animal case studies
Elucidating the perception and transduction steps in environmental cue and response systems is a major challenge, especially in the context of real- world conditions. Below, four particularly well- characterized plant and animal case studies are presented in detail, to illustrate the mechanistic complexity and ecological nuances of these systems (see Murata and Suzuki 2006 for a bacterial case study). These examples also point to the many potential avenues for ecological developmental investigation, from biochemical, molecular, and "-omics" approaches to ecological studies of multitrophic natural communities.
Light cues and plant developmental responses to shade from neighbors
Plants perceive the effects of shading by neighbors on both the spectral quality and the quantity of light they receive, through a series of distinct, partly redundant cues that integrate external and internal information (reviewed by Ballare 2009; Sultan 2010; Pierik and de Wit 2013). Light quality cues make use of the "unique property of chlorophyll- containing tissues" in strongly absorbing red light wavelengths while reflecting far-red wavelengths (H. Smith 1982, 1995); indeed humans also exploit these spectral effects to detect the presence of plant canopies, for example, in aerial vegetation surveys. For a plant, a reduced ratio of red to far-red wavelengths in light that is reflected horizontally from adjacent leaves serves as an early cue for the presence of near neighbors (Ballare et al. 1990). Once a neighbor's tissues actually begin to shade the plant, light transmitted through those tissues is also far- red enriched, prolonging and intensifying the initial signal. This signal is picked up, at both stages, by specialized phytochrome pigments located throughout the recipient plant's shoot.
These pigment molecules serve as highly sensitive detectors by switching between two photoconvertible forms, in response to small changes in the red to far-red ratio of incident light (reviewed in H. Smith 2000). This molecular switch can initiate fine-tuned, reversible growth responses within minutes of a spectral cue (H. Smith and Whitelam 1997). Interestingly, several distinct phytochrome proteins have been identified that have partly overlapping light-sensing and signaling functions; as is often the case in such "gene families," the coexistence of evolutionarily conserved and variable functional domains allows for phenotypic regulation that is at once robust and extremely precise (Schlichting and Smith 2002; Heschel et al. 2008). Phytochromes in the active molecular form are sent to the nucleus, where they bind to a group of dedicated transcription factors (phytochrome-interacting factors or PIFs) that regulate genes involved in stem and petiole elongation (Lorrain et al. 2008). Along with the red to far-red light ratio, the transcription levels of certain PIF genes are regulated by diurnal light/dark cycles and internal circadian rhythms (Salter et al. 2003; Nozue et al. 2007).
A second suite of cues signals the reduced quantity of usable light (photosynthetically active radiation) due to shade from neighboring plants. Because blue light is absorbed by plant tissues, its quantity is sharply reduced by vegetative shade, a condition perceived by specialized blue-light receptor molecules known as cryptochromes and phototropins (K. Franklin 2008). Phototropins sense the precise directionality of blue light to direct stem movements toward light and to regulate chloroplast movement within leaf cells so as to shape the spatial distribution of plastids in ways that maximize their exposure (and hence light-harvesting capacity) in low light (Ballare 2009). (As in the phytochrome family described above, phototropins encoded by homologous genes have somewhat different but partially overlapping sensitivities to blue light [Galen et al. 2004].) Along with their primary role in receiving spectral information, phytochromes may also sense reductions in the quantity of both red and far-red components of incident sunlight (Pierik and de Wit 2013). In addition to these chemical signaling mechanisms, reduced light quantity is perceived through a complex network of external and internal cues. Lower light intensity directly changes the excitation level of the Photosystem II units within leaf cells and thus influences the expression of genes involved in leaf morphogenesis (Ballare
2009). A lower flux of photosynthetically active radiation also results in a reduced concentration of carbohydrates in plant tissues; this reduction influences subsequent growth through effects on carbon storage, photosynthetic activity, and the expression of genes that influence shoot morphology (Eveland and Jackson 2012).
These light quality and quantity cues jointly initiate a well-studied complex of "shade-avoidance" growth responses that include rapid elongation of stems and petioles, more erect leaf angles, and suppressed branching (Casal and Smith 1989; Schmitt et al. 2003). In addition to PIFs, stem and petiole elongation are regulated by the DELLA family of growth-restraining proteins, which integrate several hormonal pathways. A reduced red to far-red spectral ratio leads to (1) increased biosynthesis of auxin (a key phytohormone for stem elongation) via interactions between PIF and DELLA proteins, and (2) increased ethylene synthesis, which affects DELLA stability; reduced light intensity causes an increase in gibberellins (another plant hormone with widespread effects), which promote elongation by degrading DELLAs (K. Franklin 2008 and references therein). The elongation response is also influenced by separate interactions between both ethylene and auxin with other, non-DELLA targets (Pierik et al. 2009).
This cue and response system has been exceptionally well studied in ecological context, as a primary way that plants mediate competition for light. Experimental manipulations of these signaling pathways in mutant and transgenic Arabidopsis plants grown under natural shade have confirmed that the presence and density of neighboring plants gives rise to these distinct red to far-red-ratio, blue- light, and gibberellin signals and their specific downstream effects on DELLA protein abundance and breakdown, which in turn directly regulate shoot elongation responses (Djakovic-Petrovic et al. 2007). Phenotypic manipulations (reviewed by Schmitt et al. 2003) have demonstrated that the specific developmental responses cued by neighbor shade or, alternatively, by lack of shade (and resulting light quality/quantity signals) enhance plant fitness in natural habitats and therefore constitute adaptive plasticity in response to alternative light environments (Dudley and Schmitt 1996; Donohue et al. 2000).