B
iology is experiencing the age of model systems1. Our present under-standing of genetics would have been very different if laboratories throughout the world had not agreed to concentrate their ef-forts on the fruit fly Drosophila melanogaster at the beginning of the century. Similarly, different branches of biology have adopteddistinct organisms as being particularly venient for the type of study at hand. As a con-sequence, we have considerable knowledge of the physiology of mice, the developmental biology of sea urchins, the molecular biology of Escherichia coli, and an understanding of disease resistance in tobacco. There are, of course, limits to this strategy of focusing on a
reduced number of organisms. Although it has been possible to understand their biology in depth, it is also clear that we are forfeiting any-thing more than a superficial knowledge of the overwhelming majority of living organisms.
Fortunately, research in evolutionary biol-ogy can help to broaden the scope of our investigations. All organisms were derived from a single common ancestor, which is why they share the same genetic/molecular ma-chinery. Thus, we can apply what we learn about a small number of organisms to the ma-jority – at least as long as we do not extrapo-late too far from our starting point in either ecological or phylogenetic space. The real question is how many model systems we need, and how far these generalizations can reason-ably be extended.
Arabidopsis as a model system
Arabidopsis thaliana (L.) Heynh. is a small annual, white-flowered member of the Brassi-caceae family, and is allied to other crucifers such as mustard, Brassica napus and broccoli. Arabidopsis thaliana was first adopted as a model system in plant genetics in the 1950s, largely as a target for mutagenesis studies2. More recently, A. thaliana has been the focus of physiological, developmental and genetic research that has made it the reference point for plant molecular biology3.
16 Hunter, J.P. (1998) Key innovations and the ecology of macroevolution, Trends Ecol. Evol. 13, 31–36
17 Tomlinson, P.B. (1994) Functional morphology of saccate pollen in conifers with special reference to Podocarpaceae, Int. J. Plant Sci. 155, 699–715
18 Wilson, V. and Owens, J.N. The reproductive cycle in Podocarpus totara, Am. J. Bot. (in press)
19 Tomlinson, P.B., Braggins, J.E. and Rattenbury, J.A. (1991) Pollination drop in relation to cone morphology in Podocarpaceae: a novel reproductive mechanism, Am. J. Bot. 78, 1289–1303
20 Takaso, T. and Owens, J.N. (1995) Pollination drop and microdrop secretions in Cedrus, Int. J. Plant Sci. 156, 640–649
21 Singh, H. and Owens, J.N. (1982) Sexual reproduction in grand fir (Abies grandis), Can. J. Bot. 60, 2197–2214
22 Owens, J.N., Simpson, S.J. and Molder, M. (1981) The pollination mechanism and the optimal time of pollination in Douglas-fir (Pseudotsuga menziesii), Can. J. For. Res. 11, 36–50
23 Owens, J.N., Morris, S. and Catalano, G. (1994) How the pollination mechanism and prezygotic and postzygotic events affect seed production in Larix occidentalis, Can. J. For. Res. 24, 917–927
24 Takaso, T. and Owens, J.N. (1996) Postpollination-prezygotic ovular secretions into the micropylar canal in Pseudotsuga menziesii (Pinaceae), J. Plant Res. 109, 147–160
25 Haines, R.J., Prakash, N. and Nikles, D.G. (1984) Pollination in Araucaria Juss., Aust. J. Bot. 32, 583–594
26 Eames, A.J. (1913) The morphology of Agathis australis, Ann. Bot. 27, 1–36 27 Owens, J.N. et al. (1995) The reproductive biology of Kauri (Agathis australis).
I. Pollination and prefertilization development, Int. J. Plant Sci. 156, 257–269 28 Singh, H. (1978) Embryology of Gymnosperms, Gebrüder Borntraeger
29 Colangeli, A.M. and Owens, J.N. (1989) Postdormancy seed-cone development and the pollination mechanism in western hemlock (Tsuga heterophylla), Can. J. For. Res. 19, 44–53
30 Owens, J.N. and Blake, M.D. (1983) Pollen morphology and development of the pollination mechanisms in Tsuga heterophylla and T. mertensiana, Can. J. Bot. 61, 3041–3048
31 McWilliam, J.R. (19958) The role of the micropyle in the pollination of Pinus, Bot. Gaz. (Chicago) 120, 109–117
32 Ziegler, H. (1959) Uber die Zusammensetzung des Ëbestaubungstropfensí und den Mechanismus seiner Sekretion, Planta 52, 587–599
33 Serdi-Benkaddour, R. and Chesnoy, L. (1985) Secretion and composition of the pollination drop in the Cephalotaxus drupacea (Gymnosperm,
Cephalotaxeae), in Sexual Reproduction in Higher Plants (Cristi, M., Gori, P. and Pacini, E., eds), pp. 345–350, Springer-Verlag
34 Runions, C.J. and Owens, J.N. Evidence of prezygotic self-incompatibility in a gymnosperm, in Proceedings: Reproductive Biology ’96 in Systematics, Conservation and Economic Botany (1–5 Sept. 1996), Royal Botanical Gardens, Kew, UK (in press)
John N. Owens*is at the Centre for Forest Biology, PO Box 3020 STN CSC, Victoria, BC, Canada V8W 3N5; Tokushiro Takaso is at the Iromote Station, Tropical Biosphere Research Centre, University of the Ryukyus, 870 Uehara, Taketomi-cho, Okinawa 907-1541, Japan;
C. John Runions is in the Section of Ecology and Systematics, Corson Hall, Cornell University, Ithaca, NY 14853-2701, USA.
*Author for correspondence (tel 11 250 721 7113; fax 11 250 721 6611; e-mail [email protected]).
Ecological and evolutionary
genetics of Arabidopsis
Massimo Pigliucci
The crucifer Arabidopsis thaliana has been the subject of intense research into molecular and developmental genetics. One of the consequences of having this wealth of physiological and molecular data available, is that ecologists and evolutionary biologists have begun to incorporate this model system into their studies. Current research on A. thaliana and its close relatives ably illustrates the potential for synergy between mechanistic and organismal biology. On the one hand, mechanistically oriented research can be placed in an historical context, which takes into account the particular phylogenetic history and ecology of these species. This helps us to make sense of
From the standpoint of reductionist biology, the main advantages of A. thaliana reside in its small genome and reduced number of chromo-somes; the ease with which it can be trans-formed; the fact that it is easy to grow at high density; and the fast life cycle of some of its ecotypes. The word ecotype is used loosely in the case of A. thaliana. The original use of the term4was to indicate a genetically adapted
eco-logical specialist, such as an alpine form, or a heavy metal tolerant form. Arabidopsis
thali-ana’s ecotypes are usually distinguished into
‘early’ and ‘late’ flowering, depending on the length of their vegetative phase and their type of phenology – spring ephemerals or winter annuals.
Recently, however, this species and its close relatives have also been the subject of ecological and evolutionary research5–7. The
underlying idea is to exploit the wealth of in-formation on the molecular and physiological machinery of A. thaliana to shed some light on ecological and evolutionary questions. The following review briefly summarizes what is known about the ecology and evolution of A.
thaliana and its close phylogenetic neighbors.
The ultimate aim of this is to facilitate the inte-gration of many biological disciplines and to encourage a multifaceted approach to under-standing a single group of organisms.
A simple plant?
Arabidopsis thaliana is a relatively simple
flowering plant, in that it is a typical annual weed, equipped with a minimum phenotype and characterized by a straightforward life cycle. The phenotype of A. thaliana features a filamentous root system, a basal rosette of leaves, a main flowering stem (which usually develops lateral branches), and optional ad-ditional flowering branches stemming from the base of the plant. Its life cycle is roughly divided into four stages. First, the germinating seed-ling elongates and etiolates; the cotyledons then open and the first true leaves are formed. Second, the rosette grows to a number of leaves over a period of time that varies with the popu-lation and the environmental conditions7 –
plants can produce anywhere between five to six and hundreds of leaves. Third, the main stem begins to elongate (bolting), and the first flowers open within a few days. Under favor-able environmental conditions, additional basal meristems also develop into inflorescences, so that the total fruit/seed output can vary dra-matically. Finally, leaves and fruits begin to senesce, the fruits split open, and the seeds are released. Seeds can germinate immediately or go through a period of dormancy, again de-pending on the population and the environment. This apparently simple scenario is compli-cated by a variety of responses to environmen-tal conditions, which have been the focus of much ecological research. In particular, the time
of flowering can vary considerably, thereby affecting the entire life cycle and reproduc-tive fitness of the plant. At least four groups of populations have been distinguished8. A
very early flowering kind (presumably spring ephemerals) bolts within 40 days of sowing (this includes virtually all the ecotypes used in molecular genetic research), and does not re-spond to vernalization unless grown under short days. A second type (probably early summer annuals) flowers somewhat later and responds only slightly to vernalization. In the third class (which is thought to correspond to the ecologi-cal type of late summer annuals) bolting is de-layed even further, and this effect is heightened by a lack of vernalization. The fourth group be-have as winter annuals and flower in four to six months, although this can be reduced to a sin-gle month by vernalization (e.g. 70 days at 28C). It has to be pointed out that this classification is based on physiological data alone, and that we still lack convincing field evidence that the assumed ecology of these types corresponds to their habit under natural conditions. No exam-ples of biennial A. thaliana have been described to date, although some of its relatives are bien-nial, and some genotypes do not flower within one season if exposed to short photoperiod (M. Pigliucci and H. Callahan, unpublished). From an ecological perspective it is inter-esting that there is no clear association between the flowering habit of A. thaliana and its geo-graphic distribution. Populations from both Scandinavia and Tennessee are winter-annual, as are the genotypes from warm and dry Mor-avia and wet and cold Rhineland in Europe. Furthermore, Cologne (Germany) and Grenoble (France) are characterized by similar tempera-tures and precipitation, but they host summer an-nuals and winter anan-nuals, respectively. Several genes have been found to affect both flowering time and its response to photoperiod and ver-nalization (the effect is also mediated by gib-berellic acid)9. Thus, this deceptively simple
aspect of the plant’s ecological genetics is likely to keep researchers busy for some time to come. Another supposedly established fact about
A. thaliana is that it is predominantly a
self-ing species. Interestself-ingly, this characteristic is usually invoked as an objection to its use in evolutionary studies: selfed organisms are con-sidered to be evolutionary dead-ends, because their populations do not harbor significant genetic variation. Although an estimate of the outcrossing rate of this species gave a value of 0.3% based on allozyme markers10, several
lines of evidence point to higher values (around 1.2–2.2%)11, implying that it is a more
interest-ing subject for studies on population genetics. Even the allozyme studies revealed 45 differ-ent multilocus genotypes based on seven poly-morphic loci when 470 individuals were sampled from 16 populations (with up to eight genotypes per population); these figures are
not indicative of low genetic variation. Further-more, quantitative genetic studies of several characters in A. thaliana have shown signifi-cant heritability and genetic variation both within and among populations12. Also,
mol-ecular studies using DNA sequencing of the inter-spacer (ITS) region of the chloroplast genome have revealed remarkable variation both among and within populations (M. Cruzan and M. Pigliucci, unpublished). Finally, pro-togyny may significantly contribute to out-crossing in A. thaliana (I. Al-Shehbaz, pers. commun.). Clearly, there is the need to further assess the mating system and population genetics of this species.
The complexities of weed ecology
Arabidopsis thaliana is an excellent example
of what a weed can do from an ecological stand-point. Although it is rarely locally abundant (its populations seldom count more than a few scattered individuals or clumps), and it does not withstand competition with grasses or other tall vegetation, its geographical range is none-theless impressive. The northernmost limit of its distribution is northern Scandinavia, and the southernmost tip of its range is in northern Africa and the Middle East. To date, and in spite of all we know about the physiology and molecular biology of A. thaliana, no system-atic investigation of what makes this astound-ing geographical range possible with such a ‘simple’ phenotype has been undertaken.
What is known, is that A. thaliana responds dramatically to environmental variation over a wide range of spatial scales. When used for bioassays in a series of explant trials within an area of 50 m2of undisturbed forest, it was
found that the environmental variance (meas-ured by the response of the plant) between sites, increased with distance5. However, the
correlation between sites decreased with sep-aration in the same fashion at all spatial scales examined. In other words, environments – as perceived by A. thaliana – display the same degree of complexity at all spatial scales.
An elegant experimental design was used to investigate the response of A. thaliana to selection over very short spatial scales13.
Because the distance over which the homog-enizing effect of selection occurred turned out to be very small (with random distributions above that scale), one can reasonably infer that most of A. thaliana’s ecology is local.
However, these experiments did not address the factors responsible for this extremely lo-calized response to selection. To address this point, an investigation into the spatiotemporal effects of nitrogen and litter availability was carried out14. It was found that some English
populations undergo two life cycles within a given year. Some plants flower in the spring (May–June), and their offspring do not go through dormancy, but germinate immediately and flower in late summer (September–Octo-ber). The seeds of the summer generation then overwinter, to germinate the following spring. These investigations revealed that litter from the spring individuals fosters reproductive out-put in the summer generation (mostly very small individuals responding to high density – a re-sult of phenotypic plasticity). By contrast, the overwintering seeds cannot use the litter of the previous generation because it is washed away. However, because they are at a much lower population density, they produce plants with large rosettes, which accumulate photosynthate and yield a significant number of siliques.
These experiments demonstrate how little we know about the ecology of A. thaliana. For example, we do not know how widespread the two-generation cycle is, or which ecological factors may determine its occurrence. Further-more, because there have been few experi-mental studies of A. thaliana in the field5,14,15,
we are in no position to interrelate the micro-and macro-ecology of this plant.
Phenotypic plasticity
Several laboratories have focused on the use of A. thaliana in studies on phenotypic plas-ticity – the way in which genotypes respond
to heterogeneous environmental conditions7,16.
The phytochrome genes in A. thaliana (which control response to light availability, light quality and photoperiod) are presently some of the best known examples of plasticity genes. A plasticity gene is a receptor of environmen-tal change that effects a cascade of specific and fitness-enhancing developmental/pheno-typic changes17. An investigation into the
plas-ticity of a wild-type inbred line and of several single-gene mutants representing potential plasticity genes is summarized in Fig. 1. This study demonstrates that the elimination of all of the phytochromes (which control the re-sponse to canopy shade), transforms the plas-tic wild type into a genotype that is totally unresponsive to this specific environmental change, although there is no effect on other kinds of plasticity. This lack of plasticity di-rectly translates into a proportional reduction in reproductive fitness of the mutants (which are otherwise physiologically and develop-mentally normal). This investigation demon-strates the adaptive implications of phenotypic plasticity18.
Contrary to expectations based on its puta-tive selfing habit, A. thaliana shows a tre-mendous degree of variation for phenotypic plasticity to an array of environmental circum-stances. A study of four populations (two early flowering and two late flowering ecotypes), re-vealed significant responses to water, nutrient and light gradients, with significant genetic variation among populations for several traits in reaction to nutrient and light availability19. A
larger survey of 26 populations found signifi-cant population by environment interaction (i.e. genetic variation for plasticity) for five out of nine traits20. Size-fecundity
relation-ships also varied significantly in response to light, nutrient and pot volume gradients21. This
latter study identified a minimum size thresh-old that the plant has to reach to be able to
flower. However, the value of the threshold is itself environmentally dependent (i.e. plastic). Other researchers have used A. thaliana as a model system to explore the effects of her-bivory15, and the interaction between
her-bivory and abiotic factors22. A poorly explored
aspect of plasticity in A. thaliana (and in other plants and animals as well) is the interaction between development and environment. Eco-logical studies have demonstrated develop-mental stage-specific variation for plasticity12,
and research carried out on mutants has pin-pointed the complex and antagonistic mol-ecular basis of developmental windows of plasticity23. Although a general framework for
this kind of research has not yet emerged, it is a growing area and demonstrates the trend for a direct interaction between ecological and molecular genetics.
Quantitative genetics and constraints
Arabidopsis thaliana is surprisingly
geneti-cally variable, both at the DNA sequence and at the quantitative genetic level. This has af-forded some interesting evolutionary studies of this plant. One old problem in evolutionary genetics is represented by dominance24,25. To
understand the evolution of dominance we need studies addressing both its proximate causes (the genetic and physiological bases), and its ultimate causes (i.e. under what cir-cumstances natural selection favors a certain degree of dominance). It has been shown that dominance of two mutations in A. thaliana that affect the production of abscisic acid is modulated by maternal effects26, which
pro-vides the proximate cause of dominance in this instance. This kind of work can be integrated into studies on the selective advantage of dif-ferent degrees of dominance and of the evolu-tionary dynamics of maternal effects, to yield insights into the broader question of why dominance evolves.
Fig. 1. Reaction norms for number of rosette leaves (a) and fruit production (b) in response to altered light quality [low Red (R):Far Red (FR),
on the right side of the abscissa, simulating canopy shade]. Landsberg erecta (blue line) is an inbred line used under standard laboratory con-ditions. The mutants functionally lack all phytochromes, and therefore cannot perceive red light; they are the classic hy1 (red line) and hy2 (green line) chromophore mutants, which correspond to two different loci with similar biochemical and phenotypic effects. Notice the simi-larity between the reaction norms of both wild type and mutants for the two traits.
Low R:FR Neutral shade
Treatment 17
15
13
11
9
7
5
3
Low R:FR Neutral shade
Treatment
Number of fruits
Number of leaves
250
200
150
100
50
0
Recently, quantitative genetics has ac-quired a new tool with which to merge evolu-tionary and molecular genetics. It is now possible to use molecular markers to identify and map the positions of genetic regions affecting quantitative characters in natural populations. These elements are known as Quantitative Trait Loci (QTLs)27. QTL
map-ping has been used to study phenotypic plas-ticity, flowering time and life history28,29.
However, a word of caution is necessary. If the stated goal is to investigate loci affecting life-history evolution in natural populations, it is inappropriate to compare artificially derived lines grown under continuous light30, as this is
an unnatural condition. Care has to be taken to prevent our enthusiasm for interdisciplinary research and new techniques from getting in the way of our understanding of the under-lying biology.
Another long-standing evolutionary prob-lem is the question of constraints31,32. A very
well known genetic constraint in A. thaliana is represented by a strong phenotypic and genetic correlation between flowering time and leaf production (i.e. between size and age at maturity)30,33. It is interesting that the
in-tensity of this constraint depends on the genetic background, as well as on the en-vironment in which the plant grows. It is also possible to break the constraint to some ex-tent, and obtain plants with a very different combination of the two traits compared to the wild type. This can be achieved by in-ducing mutations in different backgrounds, and then comparing the position in pheno-typic space of the mutants and the respective wild-type (Fig. 2). Such an approach rep-resents one of the first experimental attempts to address the evolutionary problem of constraints.
The big picture: evolution and systematics of Arabidopsis
No matter how interesting a model system is from a molecular or even an ecological stand-point, the crucial test of its relevance from an evolutionary perspective is provided by the exploration of its phylogenetic neighborhood. Until recently, the systematics of Arabidopsis was confusing34, but several authors have
con-centrated on revising the situation, applying modern molecular and cladistic analyses to the group34–36.
Many of the species that used to be classi-fied as being Arabidopsis are currently consid-ered as being fairly distant relatives, whereas taxa once in Arabis or Cardaminopsis are now thought of as being Arabidopsis in the strictest sense. The emerging phylogenetic picture of this genus immediately creates the opportunity to examine interesting questions from an evo-lutionary perspective. For example, A.
thali-ana is an annual, but several of its relatives are
biennials or perennials. How often does a new flowering habit emerge through history? How are these evolutionary shifts related to the ecology, and therefore what are the selective pressures these plants experience? Further-more, not all members of Arabidopsis are diploid. In fact, one of A. thaliana’s closest relatives is A. arenosa, which is a tetraploid. Recent research has confirmed an old specu-lation that A. thaliana and A. arenosa are respectively the female and male parent of a third taxon, A. suecica37,38. The wealth of
mol-ecular and physiological information available for A. thaliana opens up previously unfore-seen possibilities for investigating the ecology and evolution of hybridization and polyploidy (as well as the evolution of mating systems), because A. thaliana is predominantly self-crossing, while the other two are outcrossing.
Fig. 3. Evolution of phenotypic plasticity of leaf production in response to light quality in
Arabidopsis and allied species. The length of the bars to the right of each taxon indicates the intensity of the plastic response: the color of the bar indicates distribution in Central Europe (yellow), Eastern Europe (red) and Northern Europe (blue). Hylandra (also known as A. suecica) indicates a hybrid between A. thaliana and (presumably) A. arenosa (belonging to the Cardaminopsis clade). The phylogenetic position of A. thaliana’s ecotypes is inferred from their genetic distances. Note how strong or weak plasticity has apparently evolved more than once in the whole group.
0 20 40 60
A. thaliana – Columbia Derivative A. thaliana – Columbia
A. thaliana – Landsberg erecta A. thaliana – Landsberg A. thaliana – Nossen A. thaliana – Moscow
Hylandra Cardaminopsis petraea A. griffithiana A. pumila
Fig. 2. Relationship between bolting time
and leaf number in Arabidopsis thaliana. The solid red circles represent the three wild-type [Dijon (D), Landsberg (L) and Wassilewskija (W)] populations. All other circles (diameter proportional to re-productive fitness, measured as the num-ber of fruit produced) are EMS mutants from the (a) Dijon, (b) Landsberg and (c) Wassilewskija backgrounds. Note how genetic variation generated by mutation can dramatically alter the relationship be-tween the two traits. Also, it is interest-ing to note that – contrary to expectation – many mutants display a higher repro-ductive fitness than the wild types. This effect might be because the three wild types have been selected for a very short life cycle, which had the pleiotropic effect of reducing the reproductive output (M. Pigliucci and N. Turner, unpublished).
0 3 4 5 6 7 8 9 10 11 12
5 10 15 20 25 30
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0 500
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0 500
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0 500
Fitness L
D
W
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3 4 5 6 7 8 9 10 11 12
5 10 15 20 25 30
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Bolting time (days) L D
W
(a)
(b)
The availability of a phylogeny of the
Arabid-opsis genus and its more or less distant relatives
has also afforded some first-time comparative analyses addressing evolutionary ecological questions. One such question concerns the evo-lution of phenotypic plasticity. For example, in the case of plasticity of leaf production, a high degree of plasticity occurs in some distant rela-tives outside A. thaliana’s clade, but it is lost in early flowering taxa, only to re-evolve in late flowering ones (Fig. 3). It would be interesting to map the evolution of the known genes affect-ing floweraffect-ing time upon the same cladogram.
Can we put everything together? Attempts to unify biology have characterized the history of this discipline throughout the 20th century. One of the most important results of this trend has been the neo-darwinian syn-thesis that led to modern evolutionary theory. Recently, many people have invoked a long-awaited merger between organismal and mol-ecular/developmental biology. This goal now appears attainable thanks to the reliability, so-phistication, and low cost of modern molecular techniques. However, given the limited funding for the basic sciences, and the relatively small number of scientists that study either molecular or evolutionary biology, a true synthesis seems possible – at least at present – only by concen-trating on a few well chosen organisms. To-gether with other classical model systems, such as E. coli and Drosophila, Arabidopsis and its relatives are clearly gaining permanent status as members of this intensively studied group.
Acknowledgements
I wish to thank Jacqui Shykoff and Pierre-Henri Guyon, of the University of Paris-Sud, for their hospitality and discussions while preparing this review. Hilary Callahan, Mark Camara and Carolyn Wells have been instru-mental in developing some of the ideas dis-cussed in this paper. Melissa Brenneman, Jacqui Shykoff and Ihsan Al-Shehbaz have also made helpful comments.
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Massimo Pigliucci is at the Depts of Botany, and Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, USA
(tel 11 423 974 6221; fax 11 423 974 0978;
![Fig. 2. Relationship between bolting timeand leaf number in Arabidopsis thaliana.The solid red circles represent the threewild-type [Dijon (D), Landsberg (L) andWassilewskija (W)] populations](https://thumb-ap.123doks.com/thumbv2/123dok/1038008.929647/4.858.43.202.75.552/relationship-arabidopsis-thaliana-represent-threewild-landsberg-andwassilewskija-populations.webp)
