Download Plant Classification for Ecological Purposes: is

Annals of Botany 82 (Supplement A): 117-120, 1998
Article No. bo980723
Plant Classification for Ecological Purposes: is there a Role for Genome Size?
J. P. GRIME
Unit of Comparative Plant Ecology, Department of Animal and Plant Sciences, The University of Sheffield,
Sheffield S10 2TN, UK
Received: 19 November 1997 Returned for revision: 26 March 1998
Accepted: 17 June 1998
Genome size is a strong candidate for inclusion in the list of traits needed to devise a functional classification of plants.
To facilitate modelling and prediction of vegetation responses to regional and global changes in landuse and climate,
a distinctively ecological agenda is recommended for future research on inter-specific variation in nuclear DNA
© 1998 Annals of Botany Company
amount.
Key words: Genome size, nuclear DNA amount, plant functional types, global change.
INTRODUCTION
The relatively new science of ecology depends upon a much
older one-taxonomy. Ecological investigations are of
doubtful value if they refer to plants or animals which have
not been accurately identified. Inadequate taxonomy undermines the usefulness of ecological studies mainly because it
deprives other scientists of the opportunity to conduct
independent tests of published results.
Although taxonomy and ecology are closely linked it is
necessary to recognize that the two activities have very
different objectives. Taxonomy attaches particular importance to genetic and evolutionary relationships whereas
ecology seeks to recognize affinities between organisms that
perform similar functions or exhibit parallel responses in
contemporary ecosystems but may have quite different
evolutionary origins.
Over recent years there has been growing recognition
(Southwood, 1977; Pugh, 1980; Grime, 1988; Smith,
Shughart and Woodward, 1997) that, for ecological purposes, we require an alternative system to complement that
already provided by classical taxonomy. In this new system
organisms will be classified according to their functional
characteristics and strong emphasis will be placed upon
those features which are most consistently correlated with
success in particular types of habitat and failure in others.
Already, various schemes have been put forward and
functional classifications have been applied to organisms as
disparate as seaweeds, phytoplankton, butterflies and fungi.
Perhaps the most surprising development from this research
activity has been the extent to which similar criteria have
been found to be useful predictors of ecology in a wide
range of animals and plants.
Arguments between various protagonists seem destined
to continue for several more years before the objective-a
general functional classification of all organisms-can be
E-mail [email protected]
0305-7364/98/OA0117 + 04 $30.00/0
achieved. However, there are pressing reasons why we
should proceed as rapidly as possible to such a unified
system. Chief among these is the need to develop sound
predictive models of the consequences of regional and
global impacts of man's activities on the abundance of
individual populations of animals and plants and on the
functioning and sustainability of ecosystems. At present one
of the most severe impediments in formulating these
computer models is that we do not have a coherent basis
upon which to characterize the functional biology of the
organisms which inhabit even our commonest ecosystems.
In seeking opportunities to contribute to the development
of an ecological classification of organisms, two considerations are of paramount importance. First, it is essential that
we should recognize morphological, physiological or biochemical traits or sets of traits that are reliable predictors of
ecological responses. Second, it is necessary to establish
large databases documenting patterns of variation in the
selected traits across taxa and throughout the world.
The aim of this essay is to comment briefly on the
potential use of determinations of nuclear DNA amount in
vascular plants in current attempts to predict the responses
of vegetation to changes in landuse and climate. In order to
pursue this objective, it is necessary to consider the measures
required to establish the link between variation in genome
size and ecological patterns and processes. It is also essential
to identify the kinds of data collection and the form of
database which would permit testable predictions of
vegetation responses to climate and landuse at various
geographical scales. First, however, it may be useful to ask
a naive question 'Why has it taken so long to understand
the ecological implications of variation in genome size?'
THE LONG QUEST
In common with several other subjects which matured late
on the scientific scene, ecology has drawn heavily upon
older neighbouring disciplines when formulating its ob© 1998 Annals of Botany Company
118
Grime-PlantClassification: a Role for Genome Size?
jectives and methods. It has been argued (Grime, 1993) that
whilst many initial benefits were derived from this strategy
there has also been a disadvantage in terms of a distraction
of ecology away from its initial and defining research
objectives. The long and frustrating history of attempts to
understand the ecological significance (if any) of the wide
range of variation in genome size in the plant kingdom
appears to provide a classic example of this phenomenon.
From reviews such as those by Dover and Flavell (1982),
Cavalier-Smith (1985), Bennett (1987), Price (1988) and
Hancock (1996) it is clear that research on genome size is a
multifarious activity in which questions emanating from
genetics, molecular biology and developmental biology
have remained centre-stage and, until recently, have tended
to overwhelm the ecological perspective. From the viewpoint of ecologists this was an initially tolerable situation on
the assumption that molecular and genetic approaches
would eventually illuminate the development and organismal consequences of genome size, opening the way for
ecological developments. Unfortunately, the research trajectories of cell biology and genetics have involved a
narrowing focus in terms of the range of organisms studied
and the increasingly molecular scale of enquiry. This has not
provided an elucidation of the developmental consequences
of variation in genome size adequate for the purposes of
ecology. In particular, the understandable emphasis upon
laboratory subjects with rapid growth, short generation
times and small genomes e.g. Drosophila and Arabidopsis
has prevented the development of a comparative review of
the functional implications of large and small genomes.
If, in retrospect, the reliance of ecologists upon cell
biology as the route to a functional understanding of
variation in genome size has been misplaced, it is pertinent
to ask whether there are other areas of biology from which
useful insights into the mechanistic consequences of variation in genome size can be expected. In recent decades a
large volume of research has been conducted on plants of
various genome sizes by ecophysiologists and crop physiologists; is this work likely to resolve the ecological questions
surrounding genome size?
A simple dip-test of the use of genome size as an
ecophysiological predictor can be made by consulting the
comprehensive treatises Physiological ecology of North
American plant communities (Chabot and Mooney, 1985)
and Plantphysiological ecology (Pearcy et al., 1992). These
volumes contain no references to genome size, nor to any
correlated aspects of the cell cycle. These omissions are
perhaps surprising in view of published evidence of the
relevance of genome size to rates of cell division (Van't Hof
and Sparrow, 1963; Bennett, 1971), plant life-histories
(Bennett, 1972), the geographical distribution of crop plants
(Bennett, 1976), plant phenology (Hartsema, 1961; Grime
and Mowforth, 1982) and predictions of vegetation
responses to temperature (Grime, 1983).
Why has the comparative study of genome size not
captured the attention of ecophysiologists? The answer to
this question appears to be that plant physiologists are
primarily interested in other matters. Reference to Chabot
and Mooney (1985) reveals a long-standing and continuing
commitment to ecological investigations of plant growth
but, with rare exceptions, these studies refer exclusively to
the capture and allocation of carbon, energy, mineral
nutrients and water, or the tolerance of tissues to environmental stresses. To a remarkable extent reference is
omitted to the construction of plant tissue by the processes
of cell division and cell expansion. In our present state of
knowledge of this essential component of growth it is not
possible to assess its importance in plant ecology. We do
know, however, that meristematic activity is sensitive to
environmental controls (Kinsman et al., 1996) and there
must be a strong suspicion that interspecific differences in
DNA amount, cell size and length of the cell cycle (the three
attributes are inextricably linked-see, for example, Olmo,
1983; Bennett, 1987) have major consequences for growth
responses in plants and in cold-blooded animals and
inevitably therefore will have been subject to climatic
selection. Several investigations have been reported in
which strong correlations have been detected between
genome size, climatic variation and plant distribution
(Bennett, 1976; Levin and Funderburg, 1979; Wakamiya et
al., 1993), between genome size and the timing of leaf
growth (Grime, Shacklock and Band, 1985), between
genome size and responsiveness to year to year variation in
climate (Grime et al., 1994), and in temperate grassland
species a relationship has been established between genome
size and frost sensitivity (MacGillivray and Grime, 1995).
There is also some evidence (Thompson, 1990) that variation
in genome size coincides with differences in seed dormancy
and germination behaviour.
In view of the low penetration of cell biologists and
physiologists into problems associated with variation in
genome size the time seems ripe to set a distinctively
ecological agenda in this field of research. The concluding
section of this paper explores the measures required for such
a development.
AN ECOLOGICAL AGENDA FOR
RESEARCH ON GENOME SIZE
In seeking a model for the procedures necessary to develop
and validate an approach to utilizing genome size as an
ecological predictor it is helpful.to refer to previous attempts
to use particular plant traits in regional and global models
of vegetation distribution and responses to environmental
change. From these sources we can anticipate a need for: (1)
a comprehensive database on genome sizes; (2) complementary databases on other plant traits; and (3) tests of
predictions.
A database on genome size
Several ecologists such as Raunkiaer (1934), Box (1981)
and Woodward (1992) have recognized correlations between
plant morphology and climate and have used these as a
basis for interpretation, prediction and modelling. There
can be little doubt that the most powerful factor influencing
these approaches was the availability world-wide (as a byproduct of plant taxonomy) of standardized published
Grime-PlantClassification: a Role for Genome Size?
information on the architecture and morphology of the
dominant plants in each of the world's climatic zones. From
this experience we can draw the conclusion that success in
implementing genome size as an ecological predictor will
strongly depend upon the extent to which a database can be
constructed that includes data on the common plants of all
major habitats across the world. Here it is vitally important
that the screening of nuclear DNA amounts should not be
confined to the dominant plants at pristine locations. In
order to facilitate modelling of the dynamic responses of
vegetation to climate and landuse it is necessary to include
the weeds and other early-successional species which are
now a rampant consequence of eutrophication and disruptive landuse in tropical, temperate and semi-arid
regions.
What are the prospects for development of a database
adequate to meet these testing desiderata? There appears to
be reason for optimism. The technology for DNA measurement is now widely available and more standardized, and
through the persistent efforts of Bennett and colleagues
(Bennett and Smith, 1976, 1991; Bennett et al., 1982;
Bennett and Leitch, 1995, 1997) and many others throughout
the world, compilation of data on variation in genome size
in land plants has gathered momentum in recent years.
Complementary databases
Although some predictions of plant distribution and
responsiveness to environmental factors can be developed
from the use of genome size alone (Bennett, 1976; Grime
and Mowforth, 1982; MacGillivray and Grime, 1995) it is
likely that the full value of nuclear DNA amounts will be
realized only where these determinations can be applied in
association with other measurable plant traits. This is based
on the assertion that plant ecologies are determined by sets
of traits in which the functional significance of a large or
small genome could differ substantially according to its
genetic context. Hence, for example, the small genome of
,Arabidopsis thaliana may be part of a suite of traits
facilitating early completion of a short life-history whereas
in Chamerion angustifolium it is associated with the rapid
monopolization of resources by a clonal perennial. Different
again, is the involvement of a small genome in the long-lived
arctic sedge Eriophorum vaginatum; here we may suspect
that the short cell-cycle allows opportunistic growth in brief
episodes of warmer temperatures.
In order to decide what complementary databases are
required to fully exploit data on genome size there is a need
for urgent consideration of both key requirements and the
practicality of collecting additional data across the world
flora. Some insights into this problem are available from a
recent laboratory manual of ecological screening procedures
(Hendry and Grime, 1993). However, the scale of any such
supplementary screening is likely to be formidable and
would need to be planned with extreme caution. Here an
exciting recent development (Thompson, Band and Hodgson, 1993; Wilson and Hodgson, unpubl. res.) is the
application of techniques whereby time-consuming determinations of important ecological traits (e.g. potential
119
relative growth rate, seed bank persistence) can be replaced
by extremely rapid procedures.
Tests of predictions
Opportunities are already available on a restricted scale
to test the value of genome size as a predictor of vegetation
responses to climate. In the temperate zone most communities of herbaceous vegetation contain an array of
genome sizes in the dominant plants, and phenological
studies (Grime and Mowforth, 1982; Grime et al., 1985)
confirm that seasonal differences in canopy expansion are
often correlated with differences in genome size. In
examining the value of DNA amount as a predictor of
responses over a longer time-scale, monitoring studies such
as that conducted at Bibury in Gloucestershire, UK over a
40 year period by Professor A. J. Willis (see Grime et al.,
1994) are extremely valuable.
Unfortunately, monitoring studies are few in number and
often lack the degree of precision required for critical tests.
In consequence we may need to rely upon tests of climatic
and landuse impacts on vegetation that involve experimental
manipulations. Several experiments of the type are now in
progress in various parts of the world and can be expected
to provide excellent opportunities to evaluate genome size
as a predictor of vegetation response to global and regional
change.
LITERATURE CITED
Bennett MD. 1971. The duration of meiosis. Proceedingsof the Royal
Society of London B 178: 277-299.
Bennett MD. 1972. Nuclear DNA content and minimum generation
time in herbaceous plants. Proceedings of the Royal Society of
London B 181: 109-135.
Bennett MD. 1976. DNA amount, latitude and crop plant distribution.
Environmental and ExperimentalBotany 16: 93-108.
Bennett MD. 1987. Variation in genomic form in plants and its
ecological implications. New Phytologist 106 (supplement):
177-200.
Bennett MD, Leitch IJ. 1995. Nuclear DNA amounts in angiosperms.
Annals of Botany 76: 113-176.
Bennett MD, Leitch IJ. 1997. Nuclear DNA amounts in angiosperms-583 new estimates. Annals of Botany 80: 169-196.
Bennett MD, Smith JB. 1976. Nuclear DNA amounts in angiosperms.
Philosophical Transactionsof the Royal Society B 274: 227-274.
Bennett MD, Smith JB. 1991. Nuclear DNA amounts in angiosperms.
Philosophical Transactionsof the Royal Society of London B 334:
309-345.
Bennett MD, Smith JB, Heslop-Harrison JS. 1982. Nuclear DNA
amounts in angiosperms. Proceedings of the Royal Society of
London B 216: 179-199.
Box EO. 1981. Macroclimate and plant forms: an introduction to
predictive modelling in phytogeography. The Hague: Junk.
Cavalier-Smith T. 1985. The evolution of genome size. Chichester: John
Wiley & Sons.
Chabot BF, Mooney HA. 1985. Physiologicalecology of North American
plant communities. London: Chapman and Hall.
Dover GA, Flavell RB. 1982. Genome evolution. London: Academic
Press.
Grime JP. 1983. Prediction of weed and crop response to climate based
upon measurements of nuclear DNA content. In: Aspects of
Applied Biology 4: 87-98.
Grime JP. 1988. The C-S-R model of primary plant strategies-origins,
implications and tests. In: Gottlieb LD, Jain S, eds. Evolutionary
plant biology. London: Chapman & Hall, 371-393.
Grime JP. 1993. Ecology sans frontieres. Oikos 68: 385-392.
120
Grime-Plant Classification: a Role for Genome Size?
Grime JP, Mowforth MA. 1982. Variation in genome size-an
ecological interpretation. Nature 299: 151-153.
Grime JP, Shacklock JML, Band SR. 1985. Nuclear DNA contents,
shoot phenology and species co-existence in a limestone grassland
community. New Phytologist 100: 435-445.
Grime JP, Willis AJ, Hunt R, Dunnett NP. 1994. Climate-vegetation
relationships in the Bibury road verge experiments. In: Leigh RA,
Johnston AE, eds. Insight from foresight: Long-term experiments
in agricultural and ecological sciences. Wallingford: CAB International, 271-285.
Hancock JM. 1996. Simple sequences and the expanding genome.
BioEssays 18: 421-425.
Hartsema AM. 1961. Influence of temperature on flower formation and
flowering of bulbous and tuberous plants. In: Ruhland W, ed.
Handbuch der Pflanzenphysiologie. 16 Ansenfaktoren in Wachstum
und Entwicklung. Berlin: Springer, 123-167.
Hendry GAF, Grime JP. 1993. Methods in comparativeplant ecology-a
manual of laboratory methods. London: Chapman and Hall.
Kinsman EA, Lewis G, Davies MS, Young YE, Francis D, Thomas ID,
Chorlton KH, Ougham HJ. 1996. Effects of temperature and
elevated CO 2 on cell division in shoot meristems: differential
responses of two natural populations of Dactylis glomerata L.
Plant, Cell and Environment 19: 775-780.
Levin DA, Funderburg SW. 1979. Genome size in angiosperms;
temperate versus tropical species. American Naturalist 114:
784-795.
MacGillivray CW, Grime JP. 1995. Genome size predicts frost
resistance in British herbaceous plants: implications for rates of
vegetation response to global warming. Functional Ecology 9:
320-325.
Olmo E. 1983. Nucleotype and cell size in vertebrates; a review. Basic
and Applied Histochemistry 27: 227-256.
Pearcy RW, Ehleringer J, Mooney HA, Rundel PW. 1992. Plant
physiologicalecology. London: Chapman & Hall.
Price HJ. 1988. Nuclear DNA content variation within angiosperm
species. Evolutionary Trends in Plants 2: 53-60.
Pugh GJF. 1980. Strategies in fungal ecology. Mycological Society 75:
1-14.
Raunkiaer C. 1934. The life forms of plants and statistical plant
geography; being the collected papers of C. Raunkiaer. Translated
into English by Carter HG, Tansley AG and Miss Fansboll.
Oxford: Clarendon Press.
Smith TM, Shughart HH, Woodward FI. 1997. Plantfunctional types:
their relevance to ecosystem properties and global change. Cambridge: Cambridge University Press.
Southwood TRE. 1977. Habitat, the templet for ecological strategies.
Journal of Animal Ecology 46: 337-365.
Thompson K. 1990. Genome size, seed size and germination temperature
in herbaceous angiosperms. Evolutionary Trends in Plants 4:
113-116.
Thompson K, Band SR, Hodgson JG. 1993. Seed size and shape predict
persistence in soil. FunctionalEcology 7: 236-241.
Van't Hof J, Sparrow AH. 1963. A relationship between DNA content,
nuclear volume and minimum mitotic cycle time. Proceedings of
the National Academy of Sciences, USA 49: 897-902.
Wakamiya I, Newton RJ, Johnston JS, Price HJ. 1993. Genome size
and environmental factors in the genus Pinus. American Journalof
Botany 80: 1235-1241.
Woodward Fl. 1992. Predicting plant responses to global environmental
change. New Phytologist 122: 239-251.