Journal of Experimental Botany, Vol. 51, No. 352, pp. 1781-1788,
November 1, 2000
© 2000 Oxford University Press
Review Articles |
Annuality, perenniality and cell death
Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion SY23 3EB, Wales, UK
Received 6 June 2000; Accepted 4 August 2000
Abstract
This essay considers annuality and perenniality as quantitative traits and discusses the application of established and new genetic tools to the analysis of plant life histories. Annual/perennial status is a function of meristem determinacy in combination with the processes of cell death and disposal employed by plants to generate well-adapted anatomies and morphologies. Creeping perennials, like clover or bracken, seem to move around in the environment. They do this by extending into unoccupied space while the oldest tissues behind the growing and mature regions senesce, die and decompose. Trees do essentially the same thing, except that they develop vertically and the old dead tissue does not disappear but instead persists as wood. A root system is a kind of upended vertical perennial. The balance between exploratory growth and the wave of tissue death that succeeds it is a major determinant of perenniality. So although perenniality and annuality may appear to be dramatically different traits, extremes of behaviour can arise by a relatively minor change in the relationship between growth and death. This conclusion is supported by evidence from genome dosage studies, from the practical experiences of breeding perennial-type traits into annual backgrounds and from molecular cladistics. Applications of methods for the genetic analysis of quantitative characters are described, including the exploitation of introgression mapping in Lolium–Festuca and quantitative trait locus mapping in cereals and other species.
Key words: Cladistics, genome dosage, introgression, longevity, meristem, mapping, quantitative trait, senescence.
Introduction
For a plant to be perennial (in this discussion, ‘perennial’ generally means ‘non-annual’) the apical meristem of at least one of its shoot axes must remain indeterminate beyond the first growth season. Determinacy is usually associated with development of the floral meristem; conversely, the shoot apical meristem is normally indeterminate for as long as it remains vegetative. But there are many exceptions to these generalizations (Battey and Lyndon, 1990
), as Fig. 1 illustrates for the case of clover. Axes bearing inflorescences that are usually terminal can resume vegetative growth, as shown by the unusual genotype in Fig. 1a. The viral disease clover phyllody (Jones and Stoddart, 1971) has the effect of stimulating reproductive apices to produce leaves instead of floral organs, but these meristems remain determinate (Fig. 1b). Whilst meristem determinacy is important for annual/ perennial status, it is by no means the whole story. Progressive programmed senescence and death make critical contributions too. Here the relationship between the life-history of the whole plant and that of its constituent parts is discussed. Then annuality/perenniality as the expression of competition between apical survival and progressive tissue death is considered. This leads to two broad conclusions: (1) annuality/perenniality are probably quantitative traits, and (2) there are useful new genetic tools for analysing such traits.
|
Development by planned obsolescence
The developmental architecture of plants is based on a modular plan, and each and every module is ultimately disposable. In recent years this view of development has become integrated with the general principles of selective death as a creative force in animal differentiation and adaptation (Hengartner and Bryant, 2000). Instances of localized cell elimination in animals are abundant. To take one example, the default model for development of the limb of a bird is not the chicken's foot, but that of a duck. The embryonic chick limb has clear interdigital webs that disappear during development as a consequence of the death of particular groups of cells (Hinchliffe, 1982). Essentially, the same thing happens to make the finger-like leaflets of a palm leaf (Kaplan et al., 1982). Morphogenesis in apical meristems is currently studied almost exclusively in terms of the pattern of expression of genes that regulate cell proliferation. But localized cell death in apices and primordia is also decisive for the generation of organ form and is becoming an increasingly fruitful area for research (Calderon-Urrea and Dellaporta, 1999).
A mass of cells only becomes large and structurally complex if it has been penetrated by holes or tubes. In this way surface area keeps pace with volume and vital transport and exchange processes are sustained. Development of the biological mechanisms for creating perforations was thus an essential prerequisite for the evolution of higher plants. A senescence-like autolytic programme is present in unicellular and filamentous green algae (Park et al., 1999; Moriyasu, 1995). Fossil evidence shows that the first land plants were already actively exploiting lysigeny (intracellular dissolution of protoplasm) and schizogeny (cell separation) to differentiate conducting tissues and to shed reproductive structures and other parts (Raven, 1986). Controlled cell death, part of the developmental and adaptive armoury of plants since early in evolution, is deployed on an enormous scale in the modern flora (Dangl et al., 2000). For example, most of the biomass of a tree is dead. To generalize: cell death and disposal are universally employed by plants to generate their anatomies (inter- and intracellular apertures), and to build well-adapted morphologies.
Death in the life-cycle
The way in which programmed death can define life-form is illustrated by what may be called the horizontal and vertical variations of the perennial habit (Thomas, 1994). A creeping perennial such as white clover pushes out into new areas of the environment by proliferation at its apices, occasional branching, and subsequent elongation growth. Behind this zone of environmental invasion is a wave of cell senescence, death and necrotrophic disappearance (Gallagher et al., 1997; Turner and Pollock, 1998). Loss of apical viability may be preceded by a more or less prolonged and reversible period of proliferative arrest (Wang and Woolhouse, 1982; Bleecker and Patterson, 1997). As long as the rate of exploration and proliferation does not fall below the pace of pursuing tissue death and disappearance, the plant will persist. As the zone of death passes branch points, fragmentation occurs and a population of isolated clones develops (Fig. 2). In this way creeping perennials appear to move around their environment, very like a herd of foraging animals (and models of foraging behaviour apply effectively to clonal perennials; Stephens and Krebs, 1987; Grime and Hodgson, 1987). There are examples of very long-lived clones, for example, bracken communities that date back more than 1500 years, and there are prairie grass clones maybe twice as old as this (Molisch, 1938; Stebbins, 1958; Oinonen, 1967).
|
Turning to shrubs and trees, the same principles are at work, but with two characteristic differences. First, penetration of the environment is essentially in the vertical plane rather than horizontal. Second, the tissues that have been through programmed senescence and death, instead of disappearing through post-mortem decay, persist as mummified corpses—namely as wood. The wave of cell death moving along the shoots of woody plants is seen clearly in species such as Rhododendron (Fig. 1c
). Here the current year's growth is green and the previous year's growth suberizes and lignifies in a zone that moves up, killing axillary buds and triggering senescence and abscission of leaves as it passes.
Root systems are populations of foraging units that behave, in a sense, like inverted vertical perennials. A range of lifespans for cohorts of roots, from 2–3 weeks (apple, strawberry) to over 35 weeks (sugar maple) has been compiled (Eissenstat and Yanai, 1997). Roots that have sloughed off entire epidermal and cortical regions often retain transport functions in the stele and may even initiate new laterals from the viable pericycle (Spaeth and Cortes, 1995). This further reinforces the analogy with the shoots of woody perennials and the dynamic role of cell death in development and function.
Without labouring the point further, it can be concluded that the habits of ephemerals, annuals or perennials can be understood in terms of the extent to which apical meristems can stay at least one step ahead of the succeeding wave of cell death. This view of life-history is reminiscent of the concept of the ‘blastozone’ and ‘necrozone’ as archetypal features of morphogenesis in the earliest land plants (Hagemann, 1999).
Evolution of life cycles
Here just one of many views of the evolution of annuality/perenniality is briefly discussed as a prelude to considering the genetic basis of life-history. Age at first reproduction was emphasized as a critical determinant of the fitness of individuals (Cole, 1954). This argument was further developed (Charnov and Schaffer, 1973) by taking into account age-related differences in mortality and relative growth rate, with the conclusion that the annual or ephemeral habit would be favoured in hostile environments. Moreover, in a benign habitat, with nutrient-rich soils for example, perennials are likely to be more competitive than annuals because canopy closure and light limitation favour a life-history in which there has been some investment in long-lived vegetative biomass rather than total commitment to big-bang monocarpism. This is related to an important constraining principle, the self-thinning rule (Westoby, 1984), which identifies shorter plants as more likely to die than taller. Early-season extension growth of annuals on rich soils is generally less than that of perennials, and their likelihood to be culled correspondingly greater. Consistent with these generalizations are observations of broad correlations at the level of whole floras between, among other features, seed size (in turn a correlate of the extent of nutrient remobilization from vegetative tissues), plant height and perenniality (Leishman et al., 1995). The different relationships of perennials and annuals to the resource and stress status of the habitat and the fitness consequences of competition between the different life-forms have profound and complex implications for the dynamics of heterogeneous populations (Venable and Brown, 1993). These factors are also significant in the evolution of self (in)compatibility (Morgan et al., 1997; Pannell and Barrett, 1998).
The availability of detailed phylogenies based on cladistics and molecular systematics (Doyle, 1998) allows traits such as life-history to be put in an evolutionary context within broad or narrow taxonomic groupings. In a recent study, for example, a putative history of the genus Medicago was developed using molecular data (Bena et al., 1998). Based on parsimony rules they inferred that the ancestral form was a selfing annual and that there has been recurrent evolution in the direction of perenniality and outcrossing. Building in other assumptions gave other possible reconstructions. However, a general conclusion that can be drawn from this and other studies of life-history is that annuality and perenniality are traits that recur time and again across the taxonomic range and that, with the right selection pressure, the propensity to generate either form of phenotype can be realized without the need for large-scale genetic innovation.
Perenniality as a quantitative trait
To develop the last point further: although many genes have been described that individually participate in the progression through cell division, growth, maturity, senescence, and death, life-history looks more like a matter of the quantitative relationships between expression of these genes than of simple on–off switching. Evidence for this comes from studies of crosses between annuals and perennials. Temperate forage grasses of the genera Lolium and Festuca are good subjects for seeking the genetic basis of perenniality. There is an excellent range of longevity within the complex—from virtual ephemerals such as Lolium temulentum to extremely persistent perennials such as Festuca arundinacea.
L. temulentum is strictly annual. L. westerwoldicum, though usually treated as an annual, is a short-lived perennial which, although lacking persistency, will survive to flower again in the second and sometimes succeeding years (Fig. 1d). Inverse triploid hybrids have been created between the two species by crossing tetraploid L. temulentum (T) with diploid L. westerwoldicum (W) and diploid L. temulentum with tetraploid L. westerwoldicum (Thomas, 1995). The resulting triploid hybrids had the genomic constitutions TTW and TWW. What was not reported in the original paper is that the hybrid plantlets generated by embryo culture flowered within a very few weeks. None of the plants was allowed to set seed, but inflorescences were fixed for meiotic analysis before the plants were cut back. The TTW triploids were strictly monocarpic and all the plants died. TWW plants, on the other hand, survived the winter and flowered again the following summer. The influence of L. westerwoldicum on perenniality seems to be dose-dependent. Similarly, it was found that the degree of perenniality in progeny was related to genome dosage in a cross between annual wheat and the perennialxAgrotriticum intermediodurum (a durum wheatxThinopyrum hybrid) (Jones et al., 1999).
Barley, H. vulgare, is annual but most species in the genus Hordeum are perennial. A large number of interspecific hybrids was examined and it was discovered that perenniality is dominant over annuality in all cases (von Bothmer et al., 1983). Thinopyrum turcicum (2n=10x=70) was crossed with hexaploid bread wheat and the hybrid chromosome-doubled to produce a 16x amphiploid (I King and J Harper, unpublished results). The amphiploid, which is perennial, has been backcrossed to wheat; the backcross has the polyhaploid chromosome set of Th. turcicum plus the hexaploid complement of wheat (EEEEEAABBDD). This is also perennial and continues to flower freely after three years. It has also been reported (M Leggett, personal communication) that hybrids between annual Avena species and the perennial A. macrostachya still remain alive after 14 years.
Selective transfer of agronomically useful traits between annuals and perennials has long been a mainstay of crop improvement. An example of an annual-type character exploited to rectify a deficiency in a potentially valuable perennial crop is the introduction of high seed quality from pearl millet into perennial elephantgrass hybrids used for forage and biomass (Diz and Schank, 1993). An important instance of a perennial trait into annual backgrounds is the introduction of the stay-green or non-senescence character into sorghum. Perennials tend to have low harvest indices and reproductive sink strengths. Accordingly, the monocarpic influence that would trigger and sustain wholesale foliar senescence in an annual is weak in such plants. The vegetative tissues of perennials may also be systemically less sensitive to senescence signals. Comparison of closely-related annual and perennial species often suggests that they differ in the intrinsic rate of leaf senescence. For example, detached leaves of Lolium temulentum (annual) turn yellow significantly faster than those of the perennial Festuca pratensis and have higher rates of proteolysis (A Kingston-Smith and H Thomas, unpublished results). Grain yield in cereals is principally a reflection of starch accumulation, which relies on current photosynthate and a non-senescent canopy. Seed storage protein is generally laid down towards the end of grain fill and relies principally on recycled N from senescing vegetative tissues. The canopy is, therefore, not only the source of assimilated carbon but also an intermediate storage tissue for salvageable N (Sinclair and Sheehy, 1999).
The ideotype for a high carbohydrate grain crop such as sorghum includes a canopy with extended photosynthetic duration followed by a rapid and efficient senescence and N remobilization. Late and/or slow decline in photosynthesis is a perennial-type character that could make a big contribution to grain yield in an annual background, provided there is no unbreakable genetic linkage that prevents high levels of storage and recycling of vegetative N. Sorghum and pearl millet, staples of tropical African agriculture for over 3000 years, have been grown in a pattern of shifting cultivation and are truly multifunctional crops that are used not just for grain but also for straw (Kelly et al., 1991). In Duncan's words, sorghum ‘is a coarse, perennial grass that is treated as an annual in temperate or subtropical climes ...’ (Duncan, 1996). The practice of ratooning exploits the perennial tendencies of some land-races and cultivars of sorghum (Escalada and Plucknett, 1975). Germplasm from Sudan and Ethiopia has been an important foundation for breeding programmes aimed at increasing green leaf retention (Duncan et al., 1981). Stay-green genotypes have additional beneficial attributes, notably the capacity to continue normal grain-fill under drought conditions (Rosenow et al., 1983; Borrell and Douglas, 1996), reduced lodging and improved disease and pest resistance (Rosenow, 1984).
This dosage effect of annual and perennial genomes, and the practical experiences of breeding perennial-type green leaf retention into annual-type cereals, are entirely consistent with the view that life-form and longevity can be treated as quantitative traits for the purposes of genetic analysis.
Genetic analysis of perennials
An advantage of species from the Lolium–Festuca complex as subjects for analysing perenniality is the convenience of introgression as a powerful genetic tool in these species. Introgression substitutes a gene by its homeologue from an alien background, allowing the locus to be identified, analysed and, ultimately, isolated. Several barriers must be overcome to achieve useful introgression: pollination incompatibility mechanisms, intolerance of alien chromosomes, inability of homeologous chromosomes to pair and recombine, anonymity of the introgressed segment. Between species across the range of the Loliums and Festucas, these barriers are readily surmounted. A unique feature of alien DNA introgressed by interspecific or intergeneric hybridization in Lolium–Festuca is that it is detectable by genomic in situ hybridization (GISH; Thomas et al., 1994) and using species-specific molecular markers (King et al., 1998). A range of introgression populations has been generated, each showing segregation for many different traits. Some of these populations will be particularly useful for analysing the genetic control of perenniality.
For example, lines of Lolium temulentum were derived from a cross with L. multiflorum which in turn carried an introgression from Festuca pratensis (Thomas et al., 1999). The location of the alien segment in the L. temulentum genome was shown by GISH (Fig. 1e). Associated with this segment are Festuca-derived morphological characters; expressed genes carrying polymorphisms clearly originating in the Festuca progenitor; and Festuca-specific genomic repeat sequences (Thomas et al., 1997; I Donnison, B Hauck, H Jones, H Thomas, I King, unpublished results). These observations were made on advanced backcross lines that are substantially L. temulentum in morphology and annuality (Thomas et al., 1999). However, earlier generations in the crossing programme leading to these lines clearly segregate for longevity (G Morgan, unpublished results) and represent Lolium temulentum backgrounds with perennializing introgressions that will be identifiable via GISH and molecular markers. Figure 1f is a demonstration of what is possible with this approach, applied here to an issue related to perenniality, namely survival under stress. Genes from Festuca arundinacea (highly persistent and drought tolerant) were introgressed into Lolium multiflorum (low persistence and drought susceptible) (Humphreys and Pasakinskiene, 1996). Progeny surviving a severe drought treatment were shown to carry an introgression clearly carrying genes related to the drought-resistant trait introduced from Festuca (Fig. 1f; Humphreys et al., 1998). The corresponding genomic locus can now be identified by tagging with species-specific markers (Pasakinskiene et al., 2000).
The quantitative nature of perenniality and associated characters means that they should be analysable by genetic mapping as QTLs (quantitative trait loci). Senescence in sorghum has been approached in this way (Crasta et al., 1999). A set of recombinant inbred lines was derived from a cross between the extreme stay-green B35 and Tx430, a line with relatively high susceptibility to post-flowering drought stress. Seven stay-green QTLs were identified, three of which accounted for 42% of the variability in stay-green ratings. In a similar study on pearl millet (Howarth et al., 1994; Yadav et al., 1999; Thomas and Howarth, 2000) at least five QTLs for green leaf retention have been identified. Furthermore, up to six QTLs for leaf senescence have been observed in certain Lolium populations (Thorogood et al., 1999).
If the genetic basis of the annual/perennial character is related to a quantitative interaction between on the one hand, factors influencing apical meristem determinacy and, on the other, the pattern of progressive cell death, then some degree of correlation between corresponding QTLs might be expected. In the sorghum study (Crasta et al., 1999) one of the stay-green loci mapped on top of a maturity locus. This co-localization is consistent with the notion of life-history as an expression of programmed senescence and death in combination with apical determinacy, since meristem activity and the timing of floral induction are likely to be major components of maturity. The observation that one of the QTLs for senescence in pearl millet maps at the same position as a major QTL for flowering time (Thomas and Howarth, 2000) is similarly suggestive. A gene complex for annuality in sugar beet has been described in which bolting and its suppression was controlled by a number of genes and specific daylength requirements (Abe et al., 1997). It would be interesting to discover whether loci related to programmed death processes are part of this complex, as the ideas developed in this discussion would predict.
In conclusion, when the lifespan of Drosophila, C. elegans or mouse has been experimentally extended by a few days or weeks it often makes headlines. But for extreme contrasts in longevity combined with the potential to generate populations for mapping quantitative loci related to longevity, plants offer extreme possibilities.
Acknowledgments
This discussion of perenniality is based on a paper given at an SEB Workshop on Seasonality, organized at Reading University by Nick Battey, to whom we are grateful for the invitation to participate and for his critical reading of the manuscript. Tom Jones, John Stoddart, Terry Michaelson-Yates, and Mike Humphreys kindly provided pictures for inclusion in Fig. 1 and Suzy Shipman helped with the literature survey. IGER is sponsored by the Biotechnology and Biological Sciences Research Council.
Notes
1 To whom correspondence should be addressed. Fax: +44 1970 823242. E-mail: sid.thomas{at}bbsrc.ac.uk 
References
Abe J, Guan GP, Shimamoto Y.1997. A gene complex for annual habit in sugar beet (Beta vulgaris L.). Euphytica 94, 129–135.[Web of Science]
Battey NH, Lyndon RF.1990. Reversion of flowering. Botanical Review 56, 162–189.
Bena G, Lejeune B, Prosperi JM, Olivieri I.1998. Molecular phylogenetic approach for studying life-history evolution: the ambiguous example of the genus Medicago L. Proceedings of the Royal Society, London Series B-Biological Sciences 265, 1141–1151.
Bleecker AB, Patterson SE.1997. Last exit: senescence, abscission and meristem arrest in Arabidopsis. The Plant Cell 9, 1169–1179.[Web of Science][Medline]
Borrell AK, Douglas ACL.1996. Maintaining green leaf area in grain sorghum increases yield in a water-limited environment. In: Foale MA, Henzell RG, Kneipp JF, eds. Proceedings of the Third Australian Sorghum Conference. Melbourne: Australian Institute of Agricultural Science, Occasional Publication No. 93.
Calderon-Urrea A, Dellaporta SL.1999. Cell death and cell protection genes determine the fate of pistils in maize. Development 126, 435–441.[Abstract]
Charnov EL, Schaffer WM.1973. Life-history consequences of natural selection: Cole's result revisited. American Naturalist 107, 791–793.[Web of Science]
Cole LC.1954. The population consequences of life-history phenomena. Quarterly Review of Biology 29, 103–137.
Crasta OR, Xu WW, Rosenow DT, Mullet J, Nguyen HT.1999. Mapping of post-flowering drought resistance traits in grain sorghum: association between QTLs influencing premature senescence and maturity. Molecular and General Genetics 262, 579–588.
Dangl JL, Dietrich RA, Thomas H.2000. Cell death and senescence. In: Buchanan B, Gruissem W, Jones R, eds. Biochemistry and molecular biology of plants. ASPP, Rockville, 1044–1100.
Diz DA, Schank SC.1993. Characterization of seed producing pearl milletxelephantgrass hexaploid hybrids. Euphytica 67, 143–149.
Doyle JA.1998. Phylogeny of vascular plants. Annual Review of Ecology and Systematics 29, 567–599.[Web of Science]
Duncan RR.1996. Breeding and improvement of forage sorghums for the tropics. Advances in Agronomy 57, 161–185.
Duncan RR, Bockholt AJ, Miller FR.1981. Descriptive comparison of senescent and non-senescent sorghum genotypes. Agronomy Journal 73, 849–853.
Eissenstat DM, Yanai RD.1997. The ecology of root lifespan. Advances in Ecological Research 27, 1–60.
Escalada RG, Plucknett DL.1975. Ratoon cropping of sorghum. I. Origin, time of appearance and fate of tillers. Agronomy Journal 67, 473–478.
Gallagher JA, Volenec JJ, Turner LB, Pollock CJ.1997. Starch hydrolytic enzyme activities following defoliation of white clover. Crop Science 37, 1812–1818.
Grime JP, Hodgson JG.1987. Botanical contributions to contemporary ecological theory. New Phytologist 106, (Supplement) 283–295.
Hagemann W.1999. Towards an organismic concept of land plants: the marginal blastozone and the development of the vegetation body of selected frondose gametophytes of liverworts and ferns. Plant Systematics and Evolution 216, 81–133.
Hengartner MO, Bryant JA.2000. Apoptotic cell death: from worms to wombats ... but what about the weeds? In: Bryant JA, Hughes SG, Garland JM, eds. Programmed cell death in animals and plants. Oxford: Bios Scientific Publishers, 1–12.
Hinchliffe JR.1982. Cell death in vertebrate limb morphogenesis. Progress in Anatomy 2, 1–17.
Howarth CJ, Cavan GP, Skøt KP, Layton RHW. Hash CT, Witcombe JR.1994. Mapping QTLs (quantitative trait loci) for heat tolerance in pearl millet. In: Witcombe JR, Duncan RR, eds. Use of molecular markers in sorghum and pearl millet breeding for developing countries. Proceedings of an ODA Plant Sciences Research Programme Conference, Norwich. Overseas Development Administration.
Humphreys MW, Pasakinskiene I.1996. Chromosome painting to locate genes for drought resistance transferred from Festuca arundinacea into Lolium multiflorum. Heredity 77, 530–534.[Web of Science]
Humphreys MW, Pasakinskiene I, James AR, Thomas H.1998. Physically mapping quantitative traits for stress resistance in forage grasses. Journal of Experimental Botany 49, 1611–1618.
Jones TA, Zhang XY, Wang RRC.1999. Genome characterization of MT-2 perennial and OK-906 annual wheatx intermediate wheatgrass hybrids. Crop Science 39, 1041–1043.
Jones TWA, Stoddart JL.1971. Enzyme changes in roots of healthy and phyllody-infected white clover Trifolium repens L. Physiological Plant Pathology 1, 385–396.
Kaplan DR, Dengler NG, Dengler RE.1982. The mechanism of plication inception in palm leaves: histogenic observations on the palmate leaf of Rhapis excelsa. Canadian Journal of Botany 60, 2999–3016.
Kelly TG, Parthasarathy Rao P, Walker TS.1991. The relative value of cereal straw fodder in the semi-arid tropics of India: implications for cereal breeding programmes at ICRISAT. In: Dvorak K, ed. Social science research for agricultural technology development. CABI.
King IP, Morgan WG, Armstead IP, Harper JA, Hayward MD, Bollard A, Nash JV, Forster JW, Thomas HM.1998. Introgression mapping in the grasses. I. Introgression of Festuca pratensis chromosomes and chromosome segements into Lolium perenne. Heredity 81, 462–467.
Leishman MR, Westoby M, Jurado E.1995. Correlates of seed size variation—a comparison among 5 temperate floras. Journal of Ecology 83, 517–529.
Molisch H.1938. The longevity of plants. Lancaster, PA: Science Press.
Morgan MT, Schoen DJ, Bataillon TM.1997. The evolution of self-fertilization in perennials. American Naturalist 150, 618–638.[Web of Science][Medline]
Moriyasu Y.1995. Examination of the contribution of vacuolar proteases to intracellular protein degradation in Chara corallina. Plant Physiology 109, 1309–1315.[Abstract]
Oinonen E.1967. The correlation between the size of Finnish bracken (Pteridium aquilinum L. Kuhn) clones and certain periods of site history. Acta Forest Fennica 83, 1–51.
Pannell JR, Barrett SCH.1998. Baker's law revisited: reproductive assurance in a metapopulation. Evolution 52, 657–668.[Web of Science]
Park H, Eggink LL, Robertson RW, Hoober JK.1999. Transfer of proteins from the chloroplast to vacuoles in Chlamydomonas reinhardtii (Chlorophyta): A pathway for degradation. Journal of Phycology 35, 528–538.[Web of Science]
Pasakinskiene I, Griffiths CM, Bettany AJE, Paplauskiene V, Humphreys MW.2000. Anchored simple-sequence repeats as primers to generate species-specific DNA markers in Lolium and Festuca grasses. Theoretical and Applied Genetics 100, 384–390.
Raven JA.1986. Evolution of plant life forms. In: Givnish TJ, ed. On the economy of plant form and function. New York: Cambridge University Press, 421–492.
Rosenow DT.1984. Breeding for resistance to root and stalk rots in Texas. In: Mughogho LK, Rosenberg G, eds. Sorghum root and stalk rots, a critical review. Patancheru, India: ICRISAT, 209–217.
Rosenow DT, Quisenberry JE, Wendt CW, Clark LE.1983. Drought-tolerant sorghum and cotton germplasm. Agricultural Water Management 7, 207–222.
Sinclair TR, Sheehy JE.1999. Erect leaves and photosynthesis in rice. Science 283, 1456–1457.
Spaeth SC, Cortes PH.1995. Root cortex death and subsequent initiation and growth of lateral roots from bare steles of chickpeas. Canadian Journal of Botany 73, 253–261.
Stebbins GL.1958. Longevity, habitat and release of genetic variability in the higher plants. Cold Spring Harbor Symposia on Quantitative Biology 23, 365–378.
Stephens DW, Krebs CR.1987. Foraging theory. New Jersey: Princeton University Press.
Thomas H.1994. Aging in the plant and animal kingdoms—the role of cell death. Reviews in Clinical Gerontology 4, 5–20.
Thomas H, Howarth CJ.2000. Five ways to stay green. Journal of Experimental Botany 51, 329–337.
Thomas H, Evans C, Thomas HM, Humphreys MW, Morgan G, Hauck B, Donnison I.1997. Introgression, tagging and expression of a leaf senescence gene in Festulolium. New Phytologist 137, 29–34.
Thomas H, Morgan WG, Thomas AM, Ougham HJ.1999. Expression of the stay-green character introgressed into Lolium temulentum Ceres from a senescence mutant of Festuca pratensis. Theoretical and Applied Genetics 99, 92–99.
Thomas HM.1995. Meiosis of triploid Lolium. II. Discrepancies between the analyses of chromosome configurations at metaphase I in inverse autoallotriploid combinations. Heredity 75, 446–452.
Thomas HM. Morgan WG, Meredith MR, Humphreys MW, Thomas H, Leggett JM.1994. Identification of parental and recombined chromosomes of Lolium muliflorumxFestuca pratensis by genomic in situ hybridization. Theoretical and Applied Genetics 88, 909–913.
Thorogood D, Humphreys M, Turner L, Laroche S.1999. QTL analysis of chlorophyll breakdown in Lolium perenne. Abstracts of Plant and Animal Genome VII, San Diego, 280.
Turner LB, Pollock CJ.1998. Changes in stolon carbohydrates during winter in four varieties of white clover (Trifolium repens L.) with contrasting hardiness. Annals of Botany 81, 97–107.
Venable DL, Brown JS.1993. The population-dynamic functions of seed dispersal. Vegetatio 108, 31–55.
von Bothmer R, Flink J, Jacobsen N, Kotimaki M, Landstrom T.1983. Interspecific hybridization with cultivated barley (Hordeum vulgare L.). Hereditas 99, 219–244.[Web of Science][Medline]
Wang TL, Woolhouse HW.1982. Hormonal aspects of senescence in plant development. British Plant Growth Regulator Group Monograph 8, 5–25.
Westoby M.1984. The self-thinning rule. Advances in Botanical Research 14, 167–225.
Yadav RS, Hash CT, Bidinger FR, Howarth CJ.1999. QTL analysis and marker-assisted breeding of traits associated with drought tolerance in pearl millet. In: Ito O, O'Toole J, Hardy B, eds. Genetic improvement of rice for water-limited environments. Los Banos, The Philippines: IRRI, 211–223.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  N. L. Taylor A Century of Clover Breeding Developments in the United States Crop Sci., January 16, 2008; 48(1): 1 - 13. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. M. Williams, H. A. Ansari, S. W. Hussain, N. W. Ellison, M. L. Williamson, and I. M. Verry Hybridization and Introgression between Two Diploid Wild Relatives of White Clover, Trifolium nigrescens Viv. and T. occidentale Coombe Crop Sci., January 16, 2008; 48(1): 139 - 148. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Lammer, X. Cai, M. Arterburn, J. Chatelain, T. Murray, and S. Jones A single chromosome addition from Thinopyrum elongatum confers a polycarpic, perennial habit to annual wheat J. Exp. Bot., August 1, 2004; 55(403): 1715 - 1720. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. W. Morgan, S. A. Finlayson, K. L. Childs, J. E. Mullet, and W. L. Rooney Opportunities to Improve Adaptability and Yield in Grasses: Lessons from Sorghum Crop Sci., November 1, 2002; 42(6): 1791 - 1799. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. D. Nooden and J. P. Penney Correlative controls of senescence and plant death in Arabidopsis thaliana (Brassicaceae) J. Exp. Bot., November 1, 2001; 52(364): 2151 - 2159. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||