Development and Ecology in the Time of Systems Biology

Because development is normally studied in the laboratory, the effects of environmental stimuli are largely ignored. This situation is slowly changing with the growing recognition of changes in development that can occur under different environmental conditions. For one group of developmental biologists, those who work with plants, the effects of environmental stimuli on development have always been important, whether in the lab or in the field. Why are plant biologists more aware of the effects of environment on development? The answer is apparent to anyone who has compared a tree growing in fertile soil to one growing on a mountain top—the number and arrangement of organs that a plant will form during its lifetime are determined by environmental factors.Why doesn't animal development depend upon environmental conditions? In fact, there are numerous examples of animals whose development changes with altered environmental conditions. The spadefoot toad will develop a stronger, wider jaw in response to the drying of the ponds in which it is born. This developmental modification will allow it to cannibalize its siblings (Newman, 1992xSee all References)(Newman, 1992). The patterns on butterfly wings can change with the seasons to provide better camouflage (Nijhout, 2003xDevelopment and evolution of adaptive polyphenisms. Nijhout, H.F. Evol. Dev. 2003; 5: 9–18CrossRef | Scopus (239)See all References)(Nijhout, 2003). Still, it is rare for animals to produce more organs or new organs—they rarely grow more legs or eyes in response to environmental stimuli. This difference between plants and animals may lie primarily in their use and allocation of stem cells.In most animals, stem cells are used as a means of replenishing or repairing tissues. Examples are hematopoeitic stem cells that replenish the white and red blood cells and skin stem cells that replace sloughed-off epidermal cells. Except in rare cases, like axolotls that can regrow limbs, there are no stem cells in most animals from which entire organs can be formed. In contrast, plants depend on stem cell populations laid down in embryogenesis for almost all of their postembryonic organ formation. Stem cells in the shoot, known as the shoot apical meristem, produce all of the leaves, branches, and flowers of the mature plant, while the entire root system originates from the root apical meristem.The difference in allocation of stem cells is probably related to the difference in life strategies of plants and animals. Plants are immobile and must extract nutrients and energy from a constantly changing environment. To do so, plants retain a maximum of developmental plasticity to be able to respond to environmental changes through increasing the number or direction of branches and roots. The ability of animals to move toward nutrients and away from harmful environments probably reduces the need for postembryonic organ generation.This contrast has been brought into sharp focus with the current debate about the uses of human embryonic stem cells. These cells do, in fact, have the capacity to form entire tissues and organs. But they are only found in the embryo, whence the problem of how to procure them. Much effort is now being expended trying to coax embryonic stem cells to form different tissues and organs. This is done primarily by changing environmental stimuli and seeing how the cells react. Thus, differences in developmental responsiveness to the environment in plants and animals may be primarily a matter of the timing of deployment of embryonic versus adult stem cells. Animal and plant developmental biologists find themselves asking the same question: “How do stem cell populations respond to environmental stimuli to form the myriad of cell and tissue types found in the adult organism?”The approaches of Systems Biology are beginning to be applied to this problem. The environment is ultimately sensed at the level of the individual cell. The challenge is to determine how a stem cell differs from its progeny and how different stimuli will cause it to respond by producing different types of progeny. To address these problems from a global perspective will require new tools that can assess changes at the resolution of individual cells. Various approaches are being tried including high throughput in situ hybridization (Tomancak et al., 2002xSee all References)(Tomancak et al., 2002), tissue-specific expression of poly-A binding proteins (Roy et al., 2002xChromosomal clustering of muscle-expressed genes in Caenorhabditis elegans. Roy, P.J., Stuart, J.M., Lund, J., and Kim, S.K. Nature. 2002; 418: 975–979PubMedSee all References)(Roy et al., 2002), laser capture microdissection (Nakazono et al., 2003xLaser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types(identification of genes expressed differentially in epidermal cells or vascular tissues of maize) . Nakazono, M., Qiu, F., Borsuk, L.A., and Schnable, P.S. Plant Cell. 2003; 15: 583–596CrossRef | PubMed | Scopus (255)See all References)(Nakazono et al., 2003), and cell sorting of marked cell populations (Birnbaum et al. 2003xA gene expression map of the Arabidopsis root. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W., and Benfey, P.N. Science. 2003; 302: 1956–1960CrossRef | PubMed | Scopus (707)See all References)(Birnbaum et al. 2003). The latter three approaches are normally coupled with analysis of the extracted RNA on microarrays. The problem with all of these approaches is that they achieve a snapshot of expression in individual cells under one environmental condition. To extend them to a range of different conditions is daunting. One possible solution is an “organism array,” with many identical organisms each having different marked proteins. The organism array could be subjected to different environmental stimuli and the response recorded through an appropriate scanning device. This would give cell-specific resolution of cellular processes in real time in response to environmental stimuli. Obviously, this approach is limited by the number of organisms carrying reporter proteins tagged with different fluorophores (e.g., GFP, YFP, RFP, etc.) that one can put on a slide and is best suited to transparent organisms.A related issue at the interface of development and ecology is the nature of communities that behave like multicellular organisms. Examples are microbial communities in soil, biofilms, and the symbiotic relationships of fungal mycorhizzae and plant roots. These communities are exquisitely sensitive to their environment. Their constituents and functions change dramatically under different environmental conditions. The problem in studying these communities is that in most cases it has been impossible to know what organisms are present. For example, most of the microbes in soil cannot be cultured. This is the equivalent of trying to understand formation of an organ knowing only a tiny fraction of its cell types. Here again, Systems Biology approaches are beginning to shed light on the problem. Random shotgun sequencing is being applied to communities of microorganisms. Recent analyses of the bacteria in water from the Sargasso Sea (Venter et al., 2004xEnvironmental genome shotgun sequencing of the Sargasso Sea. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., Nelson, W. et al. Science. 2004; 304: 66–74CrossRef | PubMed | Scopus (2184)See all References)(Venter et al., 2004) or in the tailings from a mineshaft (Tyson et al., 2004xCommunity structure and metabolism through reconstruction of microbial genomes from the environment. Tyson, G.W., Chapman, J., Hugenholtz, P., Allen, E.E., Ram, R.J., Richardson, P.M., Solovyev, V.V., Rubin, E.M., Rokhsar, D.S., and Banfield, J.F. Nature. 2004; 428: 37–43CrossRef | PubMed | Scopus (1129)See all References)(Tyson et al., 2004) revealed the types and numbers of species present in each. Using a similar approach to sequencing communities growing under different environmental conditions (e.g., bacteria in rainforest soil versus desert soil) would be a way of determining how such communities change with the environment.As developmental biologists and ecologists begin to find interfaces between their fields, they will probably meet evolutionary biologists. As Leigh Van Valen once said, evolution is “the control of development by ecology” (Van Valen, 1973xFestschrift. Van Valen, L. Science. 1973; 180: 488See all ReferencesVan Valen, 1973; Gilbert 2003xSee all ReferencesGilbert 2003).