Ecology: Traits of plant invaders

NEWS & VIEWS NATURE|Vol 459|11 June 2009 Nodes a P Cdr2 X Pom1 Cdk1 Wee1 Cdr1 (inactive CDK) Nucleus Nucleeus b Cdr2 Pom1 X Wee1 Cdr1 X Cdk1 (active CDK) Figure 1 | A spatial gradient links cell size to cell division in fission yeast2,3. The Pom1 protein kinase (green) is localized to the cell cortex, with the highest concentration at the cell tips. The cell-cycle regulators Cdr2, Cdr1 and Wee1 are present in cortical nodes in the middle of the cell (blue and red dots). a, In small cells, the Pom1 gradient reaches most of the cortical nodes (blue dots). Pom1 inhibits Cdr2, preventing Cdr2 and Cdr1 from inhibiting Wee1, and allowing Wee1 to phosphorylate Cdk1, thus inactivating cyclin-dependent kinase (CDK) activity and preventing entry into mitosis. b, In long cells, the Pom1 gradient does not reach the cortical nodes (red dots), and therefore Cdr2 and Cdr1 remain active in the nodes. Cdr2 and Cdr1 inhibit Wee1, preventing phosphorylation of Cdk1 and thereby leading to activation of CDK and mitotic entry. (This simplified diagram omits several other regulators of CDK activity.) Grosjean2 and Moseley et al.3 show that Pom1 distribution strongly influences the localization of Cdr2 and the other cortical node proteins. Targeting of Pom1 to the middle of the cell reduces the amount of Cdr2 at the medial cortical nodes and is accompanied by an increase in division length. By contrast, when pom1 is deleted, the nodes are no longer restricted to the middle of the cell but rather distribute throughout the cortex of one half of the cell. Together with Cdr2 phosphorylation, this spatial regulation may contribute to control of Cdr2 by Pom1, although additional mechanisms must also regulate node distribution, because in the pom1-deleted cells active cell growth prevents the nodes from spreading to the other half of the cell. These and other experiments lead Martin and Berthelot-Grosjean and Moseley et al. to propose a model for size control of cell division in which tip-localized Pom1 generates a gradient of cortical Pom1 that regulates Cdr2 activity (Fig. 1). The idea is strikingly simple: in small cells the ‘tail’ of the Pom1 gradient overlaps with the medial Cdr2–Cdr1–Wee1 network and there is sufficient Pom1 to inhibit Cdr2, allowing active Wee1 to prevent mitotic entry (Fig. 1a). However, as the cell grows and the distance between the tips and medial region increases, a crucial length is reached at which the Pom1 gradient no longer overlaps sufficiently with Cdr2–Cdr1–Wee1; Pom1 can therefore no longer inhibit Cdr2, which is free to inhibit Wee1, leading to activation of CDK and entry into mitosis (Fig. 1b). The model is elegant, but there remain several unanswered questions. How exactly does Pom1 inhibit Cdr2? Does it phosphorylate Cdr2 in vivo, and, if so, what are the consequences of this phosphorylation? In principle, Pom1 could inhibit Cdr2 not only by changing its cellular localization or cortical dynamics, but also by directly affecting Cdr2’s proteinkinase activity, or by altering the interaction of Cdr2 with other regulators. The interphase cortical nodes are also of interest — are they ‘master integrators’ of mitosis with cytokinesis? Cells deleted for pom1 divide asymmetrically 8, owing to the abnormal distribution of the nodes and their role in cytokinesis. Because pom1 deletion mislocalizes Cdr2, and Cdr2 is necessary for the localization of many proteins to the interphase nodes, I would predict that deletion of cdr2 might restore symmetrical division to pom1deleted cells. More experiments of this nature may give further insight into the regulation of cytokinesis. Finally, it should not be ignored that, even in fission yeast, where cell geometry lends itself to the proposed Pom1–Cdr2–Cdr1–Wee1 mechanism, this is unlikely to be the only way of linking cell size to cell division1. Indeed, previous work on size control in fission yeast has implicated the ‘Cdc25 branch’ of Cdk1 regulation in this process11, so it may be time to revisit this question as well. ■ Kenneth E. Sawin is at the Wellcome Trust Centre for Cell Biology, University of Edinburgh, Edinburgh EH9 3JR, UK. e-mail: [email protected] 1. Jorgensen, P. & Tyers, M. Curr. Biol. 14, R1014–R1027 (2004). 2. Martin, S. G. & Berthelot-Grosjean, M. Nature 459, 852–856 (2009). 3. Moseley, J. B., Mayeux, A., Paoletti, A. & Nurse, P. Nature 459, 857–860 (2009). 4. Nurse, P. Nature 344, 503–508 (1990). 5. Morgan, D. O. The Cell Cycle: Principles of Control (New Science Press, 2007). 6. Breeding, C. S. et al. Mol. Biol. Cell 9, 3399–3415 (1998). 7. Kanoh, J. & Russell, P. Mol. Biol. Cell 9, 3321–3334 (1998). 8. Bähler, J. & Pringle, J. R. Genes Dev. 12, 1356–1370 (1998). 9. Morrell, J. L., Nichols, C. B. & Gould, K. L. J. Cell Sci. 117, 5293–5302 (2004). 10. Vavylonis, D., Wu, J.-Q., Hao, S., O’Shaughnessy, B. & Pollard, T. D. Science 319, 97–100 (2008). 11. Rupeš, I. Trends Genet. 18, 479–485 (2002). ECOLOGY Traits of plant invaders Tim Seastedt Many plants introduced to new habitats have fewer microbial pathogens than when in their home range, and have the ability to grow rapidly. Such a combination may make for especially troublesome immigrants. The study of invasive species is a lively, not to say contentious, area of basic and applied ecology. It remains difficult to identify the mechanisms that allow plants and animals to become abundant in new landscapes. And debate continues over whether drawing a distinction between ‘native’ and ‘non-native’ species helps in analysing the factors that affect species change1,2. In a paper in Proceedings of the National Academy of Sciences, Blumenthal and colleagues3 present an assessment of invasive-plant traits that bears on both of these issues. Most plant species identified as problematic and invasive are reported to have substantially fewer viral and fungal pathogens in introduced habitats compared with the pathogen load in their native habitats4. This alone can confer a © 2009 Macmillan Publishers Limited. All rights reserved competitive advantage in new environments. Blumenthal et al. looked at 243 species of European plant that have become established in the United States. They show that the species that have probably lost the most viruses and fungi are also likely to be species capable of rapid growth, and are often good competitors under conditions of high resource availability. The authors argue that this combination of release from enemies and inherent growth ability produces a synergistic effect that explains patterns seen in the abundance and types of invaders, and in the patterns of invasion seen in many ecosystems. Ecologists often group plants by the ability of species to persist in either resource-rich environments (‘competitors’) or resource-poor environments (‘stress tolerators’). A second 783 NEWS & VIEWS comparison separates species able to exploit physical disturbances (‘ruderals’) from the other two groups5. When Blumenthal et al.3 compared pathogen numbers on these plants, an unexpected finding was that, in their home range, plants classified as competitors averaged four times as many pathogenic fungi and about seven times as many viruses as plants adapted as stress-tolerators or as stress-tolerant ruderals. The authors then looked at the question of what best explains the number of pathogen species as well as the subsequent loss of this pathogen burden when plants move to new environments. They used a scoring procedure of plant characteristics that ranked species as competitors, stress tolerators, ruderals or intermediates. They also ranked resources (light, water, nitrogen) from sample locations. Plant characteristics best explained numbers of pathogens as well as the losses in numbers of pathogens; the pathogen burden, and its subsequent reduction, was related to resource availability. Plants adapted to moderate- and highresource communities are able to grow rapidly when presented with resource opportunities6. But the fact that such plants exhibit these growth characteristics in their home environment while possessing relatively high numbers of viral and fungal pathogens is surprising. Clearly, the plants can keep pathogens in check while competing in relatively high-resource areas. In contrast, stress-tolerant plants that persist in environments that are ‘too dry’ or ‘too wet’ do so while hosting fewer pathogens. The causal relationships among these factors can be only speculative. But it seems that a resource-rich environment allows a plant to carry a higher pathogen load and persist, whereas in low-resource areas natural selection favours only those that maintain reduced pathogen loads. Plants with a growth strategy that provides quick benefits from their tissues can tolerate a higher pathogen load; in low-resource areas they need tissues that will discourage pathogen presence. These interpretations seem to be consistent with the principles of leaf and plant economics6,7 that govern the adaptive balance between growth and defence. Plant growth rates are strongly correlated with higher specific leaf area (thinner leaves) and higher foliar nutrients, and invasive plants are more likely to have these traits and therefore to grow faster8. Thus, instead of two separate mechanisms — high growth favours invaders; escape from enemies favours invaders — Blumenthal et al.3 find that both of these traits are embodied in plants that become successful invaders. This study did not rank invaders in terms of their ability to achieve extreme dominance or ‘monoculture’ in their new environments, and it would be interesting to know which plants — the competitors or the ruderals — have become the ‘worst’ invaders. Other points to consider are that viruses and fungi are not on the radar screens of many ecologists, and for 784 NATURE|Vol 459|11 June 2009 them, ‘escape from enemies’ evokes images of escape from vertebrate and invertebrate herbivores. The ‘enemies list’ for these plants contains many not included in Blumenthal and colleagues’ analysis; in escaping from microbial pathogens, many species will have escaped from their specialist herbivores as well9. Finally, the authors’ model does not consider the ‘new friends list’ — the beneficial, free-living microbes or symbionts that are acquired in the new environment, and that can also provide positive feedback to plant growth10. Invasive plants are not unique in terms of their growth physiologies; rather, these species often group within the set of plants associated with rapid-growth strategies 8. Using this criterion, the argument that invasive species are fundamentally different from native species is not justified. But Blumenthal and colleagues’ analysis3 shows that nonnative species combine two characteristics — rapid growth and a lower pathogen burden (and, presumably, fewer herbivores) — that distinguishes them from native species. Thus, the combination of the two traits does set this group apart, with a subset of them possessing extreme growth and competitive potential. Accordingly, these results constitute good evidence for the existence of a subset of nonnative species that are unique in their invasive abilities. They justify the use of the ‘non-native’ label in discussions on environmental management and biodiversity concerns, and more generally are a further step in the maturation of invasion biology as a predictive science. ■ Tim Seastedt is in the Department of Ecology and Evolutionary Biology, and at INSTAAR, University of Colorado, Boulder, Colorado 80309, USA. e-mail: [email protected] 1. Warren, C. R. Prog. Hum. Geogr. 31, 427–446 (2007). 2. Richardson, D. M., Pyšek, P., Simberloff, D., Rejmánek, M. & Mader, A. D. Prog. Hum. Geogr. 32, 295–298 (2008). 3. Blumenthal, D., Mitchell, C. E., Pyšek, P. & Jarošík, V. Proc. Natl Acad. Sci. USA 106, 7899–7904 (2009). 4. Mitchell, C. E. & Power, A. G. Nature 421, 625–627 (2003). 5. Grimm, J. P. Am. Nat. 111, 1169–1194 (1977). 6. Westoby, M., Falster, D. S., Moles, A. T., Vesk, P. A. & Wright, I. J. Annu. Rev. Ecol. Syst. 33, 125–159 (2002). 7. Wright, I. J. et al. Nature 428, 821–827 (2004). 8. Leishman, M. R., Haslehurst, T., Ares, A. & Baruch, Z. New Phytol. 176, 635–643 (2007). 9. Keane, R. M. & Crawley, M. J. Trends Ecol. Evol. 17, 164–170 (2002). 10. Mitchell, C. E. et al. Ecol. Lett. 9, 726–740 (2006). IMMUNOLOGY Immunity’s ancient arms Gary W. Litman and John P. Cannon Diverse receptors on two types of cell mediate adaptive immunity in jawed vertebrates. In the lamprey, a jawless vertebrate, immunity is likewise compartmentalized but the molecular mechanics are very different. About 500 million years ago, vertebrates divided into two forms marked by the possession or lack of jaws. Today, the jawed forms are by far the more common and include organisms as diverse as humans and sharks. Immunology research has understandably centred on the jawed vertebrates, in which it has long been known that adaptive (inducible) immunity is mainly accounted for by two distinct lineages of lymphocyte: T cells and B cells. But any understanding of vertebrate immunity has to consider our distant jawless cousins, which today are represented by only the lamprey and hagfish. On page 796 of this issue, Gou and colleagues1 do just that, and extend our concepts of the two-component nature of immune function2 through their investigation of the cellular basis of immunity in the lamprey. The business ends of T and B cells are the components that recognize foreign antigen — respectively, the T-cell antigen-binding receptor (TCR), and the B-cell receptor, which is a membrane-anchored immunoglobulin that is subsequently released as a circulating antibody (Fig. 1a). Extraordinary diversity can be generated in both TCRs and immunoglobulins outside the germline through somatic © 2009 Macmillan Publishers Limited. All rights reserved recombination, and also through hypervariation, in the case of immunoglobulins. Consequently, T and B cells can produce an immune response to all manner of invaders. One major (cellular) type of T-cell response involves killing host cells infected by viruses or bacteria. By contrast, the (humoral) B-cell-derived response consists of the production of antibodies that largely recognize and ultimately help to destroy aliens in the bloodstream. But jawless vertebrates have much to offer immunologists. Lampreys have been shown to mount an adaptive form of specific humoral immunity to Gram-negative bacteria, as well as to a determinant unique to human type O red blood cells3. Despite the antigenic complexity of the red-blood-cell surface, induced molecules that agglutinated type O blood cells did not agglutinate type A or B cells. Furthermore, the molecular size of the reactive molecules was inconsistent with that of the immunoglobulins3. Experimental strategies, based on knowledge of the genes encoding immunoglobulins and TCRs, failed to detect the evolutionary equivalents (orthologues) of these molecules in jawless vertebrates. These negative results became understandable with the recognition that