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On the life strategies of plants and animals
TIG-June
1985
perspective On the life strategies of plants-" and animals
The most important difference between higher plants and animals with respect to survival is that animals move and plants do not. If an animal encounters a threat, it can flee; Virginia Walbot animal behavior and physiology depend on cell movement (blood cells, cell of the There is a renaissance of interest in the genetics of higher plants fueled in pa'rt by the likelihaxt of improvements in crop spex'~ through genetic engineering. This has immune response) as well as emphasized the needfor modern biologists to know more about the life history and organ. the movement of the whole ization of plants. This brief essay highlights some of the profound differences between creature. By contrast, in plants higher plants and animals and addresses questions about the relationship between the neither the whole organism nor generation of genomic variation and the developmental plan of higher plants. the individual cells move. Consequently, when plants encounter stress, physiological changes have to be the principal forms of defense. rearrangements (ontogeny of the antibody producing Changes on a time scale varying from seconds to days lineages). Although many animal taxa retain the capaallow them to cope in the short term, while over a time city to reform tissues and organs after injury- such as scale of days to a full growing season, they respond to the regeneration of limbs in ~lamanders or the rea variable environment by producing new organs growth of liver in mammals - formation of a complete better-adapted to the existing environmental organism appears to depend on the union of gametes" conditions. For example, many plant species respond in a zygote. The gametes contain an intact genome to a shady environment by producing large, intensely and cytoplasmic information required to program green shade-leaves to maximize light capture; the development; they differentiate only from the germ same plant may produce smaller, more wax-covered line cells. sun-leaves to minimize water loss in intense light. The Plants have no formal germ line but their reproducbody of a plant is continuously expanding by the tion includes two distinct life phases: the haploid repetitive production of the basic organ systems and gametophyte which produces the gametes and the the morphology of the individual organs is influenced diploid sporophyte which contains cells that can by local environmental conditions during undergo meiosis. This switch from haploid to diploid organogenesis. phases is termed the alternation of generations. In A second major distinction between plants and lower plants, the gametophyte is often the dominant animals is that animals contain a germ line, a group of life phase while in higher plants it is much reduced. In cells often derived from a specialized region of the an angiosperm, the haploid phase includes the pollen zygote which migrate to the gonads. These germ cells grain containing several cells two of which serve as are generally inactive in the somatic body of the sperm and the embryo sac which is a multinucleate or animal. In contrast, the gametes of plants differentiate multicelled structure including the egg. late in development from a population of cells that After fertilization in higher plants, embryonic have been actively engaged in organizing the somatic development establishes the basic body plan of a body of the plant. The gametes are produced at the root-shoot axis. The first examples of adult tissue and periphery of the plant from cells which may have pro- organ systems soon differentiate; these include the liferated for many months or years in a vegetative root, the stem and the leaves. In contrast to animals, a mode. The situation would be comparable to the pro- plant embryo contains only a fraction of the comduction of animal gametes from the skin. What are the ponents of the final body and, furthermore, there are consequences of these differences between plant and neither reproductive structures nor a germ line. At animal life strategies? Before discussing these issues I germination a plant embryo grows by division and will present some background information on the enlargement of pre-existing cells to form a seedling developmental strategy of higher plants. and then initiates organ proliferation from stem cell Embryo development in vertebrate and inverte- populations called apical meristems. The apical meribrate animals results in a nearly complete, but often stems allow the plant to continuously produce new smaller, version of the adult body. The basic body plan organs and this meristematic activity also produces is established in the embryo (or larval stages) and more meristem tissue. includes the number and position of appendages, a The root apical meristem is near the root tip; cell germ line and stem-cell populations to replenish short- division at the distal edge of this meristem produces lived tissues. Postembryonic development often root cap cells and proximal cell divisions add to a zone involves growth of the whole animal, the completion of cell proliferation next to the meristem (see Fig. 1). of the development of pre-existing organ systems In this zone of proliferation, substantial cell division such as the gonads and the maturation of functional increases the number of cells in the root; at the proxceils from stem-cell populations. The gametes dif- imal edge of this region, cells enter a zone of elongaferentiate from a population of cells which was tion in which most of the visible increase in root length typicallyset aside early in embryonic life; the presence occurs; the elongated cells then enter a zone of cell of a germ line allows irreversible somatic differentia- differentiation in which the final functional specialization in some animal tissues, such as loss of the nucleus tions of the individual cells become apparent. The (erythropoiesis in mammals), loss of chromatin pericycle, a cylindrical tissue surrounding the central (in Ascaris embryos) or nonconservative genomic core of vascular tissue in the root, is the usual source of © 1~,5, Elaevler Science lauhlisher~ B.V.. A m ~ e r c h ~ 0168 - 9S2,5/85t$02.00
prspectives
TIG -- June t 9 8 5
branch roots; root apices form from pericycle tissue, expand through the existing root tissue and emerge into the soil. Thus, the extension growth of the original root, organized by the root apical meristem, results in a continuously elongating root with an everincreasing supply of pericycle, the source of lateral roots. The shoot apical meristem provides the initial cells forming the stem and leaves of the plant. Localized cell divisions in this apex result in lateral bulges on the meristem called leaf primordia (see Fig. 2). Active apices are encased by a whorl of developing leaves, with the youngest leaves closest to the apex; the placement of the leaves, the phyllotactic pattern, is a species-specific character. On the upper side of the junction (the axil), between each leaf primordium and the stem, a new apical meristem forms concomitant with leaf initiation in most species. Thus, organogenesis in the stem is accompanied by the proliferation of apical meristems. These axillary meristems are buds, meristems which will organize a branch when growth is initiated. Each bud contains progeny of some of the original apical meristem ceils. In summary, the major features of plant development are a perpetual stem cell population (the apical meristems), repetitive production of more organs and, as a consequence of organ production, formation of more meristems. (For further information on the general principles of plant development see Ref. 1.)
Somatic sectoring in plants Fig. 1. Structure of the root tip in longn'tudinal section.
Fig. 2. Structure of the shoot tz]~of lilac ¢Syring~ in longitudinal section. A, apical merister~" AB, young axillary bud, PH, successively older leaf ~'#~rdi~,'.
Casual observation of cultivated plants shows that variegation is common during plant growth: for example, variegated ivy. Such color variegation can arise if somatic mutation occurs in one cell of the several hundred in the apical meristem (see Fig. 3) resulting in an inability to accumulate chlorophyll in progeny cells. Initially there will be a narrow sector of albino tissue on the main axis of the plant; in some branches this sector will expand because the albino cells represent a larger fraction of the cells in the axillary meristem than in the original meristem. (For information on cell lineage analysis in maize see Ref. 2 and for an overview of chimeras and cell lineage analysis in dicotyledons see Ref. 3.) Somatic changes, initially affecting just one branch on a tree, can be of great commercial importance. Many modern varieties of fruit such as the McIntosh apple and varieties of pink grapefruit were discovered as bud sports, buds producing fruit with a novel phenotype. Bud sports are propagated by grafting and are usually true to type, each graft continuing to produce the desirable fruit characteristics. In some bud sports, the novel characteristics are not transmitted in sexual crosses; sometimes the novel fruit is sterile (many apple varieties), or the bud sport may be epigenetic and the special characteristics are lost when a new embryo is formed. In other cases (such as some varieties of pink grapefruit) sexual crosses demonstrate that the bud sport resulted from a single mutation. F l o w e r formation The shoot apical meristems produce vegetative tissue until an environmental signal triggers a switch to floral development. Individual apices cease produc-
perspective
TIG - - June 1985
tion of leaf primordia, reprogram gene expression and switch to the production of the modified leaf structures that make up the flower: sepals, petals, stamens and pistils. During vegetative growth the meristem remains approximately constant in size; cell recruitment into organs is matched by cell divisions that replenish the meristem cell population in much the same way that stem cell populations in animals are maintained at a constant cell number. During floral development, however, the cells of an apical meristem differentiate into organs and no new meristems are made. Consequently, flowers terminate a stem, preventing the apical meristem from contributing further
~Anther S~amen~ ~,Filament - - ~ } 1
II~Style
Stigma1 I Pistil
(e)
(~
Zoneof mutantcells
Remainsof styleandstigma-
-
Seed
C a r p e ~ SepalsJ
'~.g (b)
Fruitwall (derivedfromovary)- ~ N (c)
Fig. 4. Structure of a completeflower (a) and the derivation of a fruit from the ovary of theflower (b and c).
Fig. 3. An apical meri,stem produces pairs of opposite leaves, each leaf derimt from about one-fourth of the apex (a). A mutant lineage (stippled area) in the meristem is represented in only one leaf of each group of four; affected leaves are all in the same rank when the plant is viewedfrom the apex. A branch arising from the axil of an affected leaf will ogntain a much larger mutant sector than the original stem, while buds in the axils of the unmarked leaoes will contain only normal d.~sue (b).
to the vegetative body. Because floral organs are more numerous and more closely spaced than are the leaves on the stem, it is likely that cell differentiation occurs more rapidly than cel/proliferation in the floral meristem. Progresswe differentiation of floral structures occurs from the base to the tip of the meristem of the floral apex (see Fig. 4). The stamen (pollen-bearing organ) and pistil (ovary-containing organ) are the most centrally located and differentiate last; in many species the gametes are drawn from a small subset of the original apical cells2.3. Thus, in plants the floral structures equivalent to the animal gonad and germ line are derived from apical meristem cells that were previously involved in organizing the somatic body of the plant. Facile reprogramming of somatic tissue into reproductive tissue must occur in plants; in annual plants most (if not all) of the apices are converted to floral structures while in perennial plants, a subset of apices are converted from vegetative to floral development leaving a residual population of buds to support the next year's vegetative growth. The most important consequence of the mode of reproduction of plants is that the gametes differentiate at the periphery of the plant from many cell lineages. Furthermore, because ax/llary buds represent a subset of the apical cells of the branch from which they arose, a single mutant apical meristem cell !n the original shoot apex can later represent an everincreasing percentage of the ceils in a branch. It is not difficult to imagine how bud sports arise on secondary or tertiary branches. The visible phenotypic changes must represent only a small fraction of the diversity of genomes present in the cell lineages forming the various flowers of a plant. With each succeeding cell division in the shoot apices of the plant, the diversity of 1 6 ~
pspectives
the lineages should increase as a result of somatic mutation, genomic rearrangements, activation of cryptic transposable elements and other means for generating genomic change.
TIG - - June 1985
such a stringent barrier, there may be great redundancy of function in plant genes such that any one function is likely to be represented by more than one gene in the haploid generation. This would mean that mutation of one allele could be compensated for by others with the same function. The high fraction of plants of recognizable polyploid origin may be particularly well buffered against gametophytic-lethal mutations. Furthermore, mutant cell lineages are in a sense tested somatically before the germ line differentiates. If a mutation in an apical meristem cell is lethal, that cell produces no somatic tissue and its progeny are not represented in the apical meristem. Mutations with little effect on cell fitness, such as albinism, will be extensively propagated in the somatic tissue before gamete formation. But a totally albino branch cannot photosynthesize and must import fixed carbon from other parts of the plant. Stewart has suggested 3 that there is extensive competition between lineages in visible chimeras; branches which grow rapidly will produce more axillary buds and can produce more flowers from the larger population of apices. Thus, some selection on the fitness of the somatic body is possible before the formation of gametes in a particular region of the plant. In some ways, a plant body is more like a population of animals than a single animal. Each apex could be considered to be a new individual which will grow and produce additional apices, in fact considerable physiologicaldata suggest that plants are composed of semiautonomous units ~. Some of the differences among individual branches may reflect genetic changes varying from gross karyotypic changes to mutations in single genes. Because plants respond to a variable environment by constant proliferation of organs differentiating in response to the environmental conditions existing at the time of organogenesis, the diversification of the apical meristems producing the somatic body of the plant may represent one of the strategies used by plants to increase the likelihood of producing appropriate organs.
D i v e r s i f i c a t i o n of the plant genome d u r i n g continuous somatic development Two important features of plants impinge on their survival after periods of genomic change: their great tolerance of karyotypic abnormalities and the existence of a haploid gametophytic generation. The influences of these two features are conflicting in terms of their impact on adaptionperse. However, the balance between them may depend on the relationship between the amount of vegetative growth involved in exploitation ofgenomic diversity in a variable environment and the success of reproduction by individual flowers. Lower reproduction efficiency would be the price pal0 for culling unfit haploid genotypes from the gametophytic generation. Considerable evidence suggests that normal development in plants is more tolerant of genetic imbalance than in animals4. For example, abnormal karyotypes are tolerated in many species, with monosomics and trisomics producing nearly normal but semisterile individuals; interspecific and intergeneric crosses often produce viable progeny. There are fewer than 100 polyploid insect species and polyploidy in vertebrates is confined to a few fish, amphibian and reptilian groups s. However, among higher plants, polyploidy is common in the ferns, occurs in about 5% of gymnosperms, 45% of dicotyledonous plants and 55% of monocotyledonous plants; polyploidization is hypothesized to result from production of unreduced gametes. The triploid and higher ploidy karyotypes which arise from sexual crosses involving unreduced gametes must be reasonably successful to be so well represented among the extant species of higher plants. An obvious question, for which we have no answer at present, is whether plant embryo development is relatively insensitive to karyotypic alterations because such changes are common and plants have evolved appropriate chromosomal and developmental controls to reduce their effects. Such tolerance might Evidence for genetic change within plants There have been few tests of the diversity of the be selected for in plants because the individual somatic lineages may diversify within the vegetative genome within a plant 4. Plants regenerated from individual resulting in gametes with a variety of tissue culture often show considerable diversity of genomic alterations. In higher animals there may be phenotype and genotype; this variation is known as great genetic diversifications within the somatic body somaclonal variation and may reflect both the prewhich affects the fitness of the individual (i.e. karyotic existing diversity of cells in the explant and additional changes in cancerous cells). However, such genomic genomic change occurring (or even induced) during diversity is not captured in the gametes and normal tissue culture. Rapid genomic change has been embryo development appears to require a normal detected between plant generations, for example in flax plants derived from parents exposed to different genome. In all plants, there is a distinct, genetically active environmental regimes s and in crosses between haploid phase of the life cycle; in higher animals there inbred lines of maize9. B. Schaal and her colleagues at are few cases of haploid cell genetic function or Washington University, St Louis, have examined the haploid cell-limited gene products. The requirement number and organization of the ribosomal genes in for independent function of the haploid gametophyte Solidago, a long-lived perennial plant, and found in plants may eliminate many lethal genes from the evidence for changes within the individual by population by selection in the haploid rather than sampling different branches (B. Schaal, personal diploid phase of the life cycle. Genetic diversification communication). Stress has been shown to induce in the somatic body may be tolerated or even adaptive cryptic transposable elements in maize ~°'~ and in the vegetative body, but lethal in the gametophyte. McClintock proposed that stress may trigger a Alternatively, because the gametophyte presents restructuring of the maize genome ~2.
TIG -- June 1985
It is possible that the developmental strategy of the plant includes the capacity to generate and tolerate diversity among the shoot apical meristems. Growth and age would both increase the likelihood of genomic changes being represented in bud sports and of genetically different offspring being produced by individual flowers. Stress may simply increase the frequency of such changes or allow more rapid selection of novel phenotypes at the somatic level, thus increasing the probability of finding genomic changes in the subsequent generation. Clearly the developmental strategy of higher plants is very different from that of higher, motile animals. Several interesting questions for research are raised by an appreciation of these differences, particularly regarding the relationship between phenotypic plasticity and change in plants and the selection and fixation of mutation in plants. Much more research will be required in order to understand the interplay between the strategy of plant development, the lack of a germ line, the constant proliferation of apical meristems, the presence of a haploid gametophytic generation and the tolerance of genomic diversity in plants.
Acknowledgements I wish to thank Paul Green for his helpful comments on plant development and Julie Wool for her assistance in preparing the manuscript. Research support was obtained from the National Institutes of Health (GM 32422).
References
perspective
1 Steeves, T. A. and Sussex, I. M. (1970) Patterns in Plant Development, 302 pp., Prentice Hall 2 Coe, E. H., Jr and Neuffer, M. G. (1978) Embryo ceils and their destinies in the corn plant. In The Clanal Basis of Development (Subtelny, S. and Sussex, I. M. eds), pp. 113-129, Academic Press 3 Stewart, R. N. (1978) Ontogeny of the primary body in chimeral forms of higher plants. In The Clonal Basis of De~lopment (Subtelny, S. and Sussex, I. M., eds), pp. 131-160, Academic Press 4 Walbot, V. and Cullis, C. A. Rapid genomic change in higher plants. Annu. Rev. Plant Physiology, in press 5 Lewis, W. H., ed. (1980) Polyploidy: Biological Relevance, Plenum Press 6 Watson, M. A. and Casper, B. B. (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Annu. Rev. EcoL Syst. 15, 233-258 7 Larkin, P. J. and Scowcroft, W. R. (1981) Somaclonal variation - a novel source of variability from cell cultures for plant improvement. Theor. Appl. Genet. 60, 197-214 8 Cullis, C. A. (1983) Environmentally induced DNA changes in plants. CRC Crit. Rev. Pl. Sc/. 1,117-131 9 Rivin, C. J. and Cullis, C. A. (1983) Modulation of repetitive DNA in the maize genome. Genetics 104, 859-860 (and unpublished data) 10 McClintock, B. (1978) Mechanisms that rapidly reorganize the genome. Stadler Genet. Syrup. 10, 25-48 11 Burr, B. and Burr, F. (1981) Transposable elements and genetic instabilities in crop plants. Stadler Genet. Syrup. 13, 115-128 12 McClintock, B. (1984) The significance of responses of the genome to challenge. Science 226, 792-801 K Walbot is at the Department of Biological Sciences, Stanford University, Stanford, CA 94305, USA.
1985
perspective On the life strategies of plants-" and animals
The most important difference between higher plants and animals with respect to survival is that animals move and plants do not. If an animal encounters a threat, it can flee; Virginia Walbot animal behavior and physiology depend on cell movement (blood cells, cell of the There is a renaissance of interest in the genetics of higher plants fueled in pa'rt by the likelihaxt of improvements in crop spex'~ through genetic engineering. This has immune response) as well as emphasized the needfor modern biologists to know more about the life history and organ. the movement of the whole ization of plants. This brief essay highlights some of the profound differences between creature. By contrast, in plants higher plants and animals and addresses questions about the relationship between the neither the whole organism nor generation of genomic variation and the developmental plan of higher plants. the individual cells move. Consequently, when plants encounter stress, physiological changes have to be the principal forms of defense. rearrangements (ontogeny of the antibody producing Changes on a time scale varying from seconds to days lineages). Although many animal taxa retain the capaallow them to cope in the short term, while over a time city to reform tissues and organs after injury- such as scale of days to a full growing season, they respond to the regeneration of limbs in ~lamanders or the rea variable environment by producing new organs growth of liver in mammals - formation of a complete better-adapted to the existing environmental organism appears to depend on the union of gametes" conditions. For example, many plant species respond in a zygote. The gametes contain an intact genome to a shady environment by producing large, intensely and cytoplasmic information required to program green shade-leaves to maximize light capture; the development; they differentiate only from the germ same plant may produce smaller, more wax-covered line cells. sun-leaves to minimize water loss in intense light. The Plants have no formal germ line but their reproducbody of a plant is continuously expanding by the tion includes two distinct life phases: the haploid repetitive production of the basic organ systems and gametophyte which produces the gametes and the the morphology of the individual organs is influenced diploid sporophyte which contains cells that can by local environmental conditions during undergo meiosis. This switch from haploid to diploid organogenesis. phases is termed the alternation of generations. In A second major distinction between plants and lower plants, the gametophyte is often the dominant animals is that animals contain a germ line, a group of life phase while in higher plants it is much reduced. In cells often derived from a specialized region of the an angiosperm, the haploid phase includes the pollen zygote which migrate to the gonads. These germ cells grain containing several cells two of which serve as are generally inactive in the somatic body of the sperm and the embryo sac which is a multinucleate or animal. In contrast, the gametes of plants differentiate multicelled structure including the egg. late in development from a population of cells that After fertilization in higher plants, embryonic have been actively engaged in organizing the somatic development establishes the basic body plan of a body of the plant. The gametes are produced at the root-shoot axis. The first examples of adult tissue and periphery of the plant from cells which may have pro- organ systems soon differentiate; these include the liferated for many months or years in a vegetative root, the stem and the leaves. In contrast to animals, a mode. The situation would be comparable to the pro- plant embryo contains only a fraction of the comduction of animal gametes from the skin. What are the ponents of the final body and, furthermore, there are consequences of these differences between plant and neither reproductive structures nor a germ line. At animal life strategies? Before discussing these issues I germination a plant embryo grows by division and will present some background information on the enlargement of pre-existing cells to form a seedling developmental strategy of higher plants. and then initiates organ proliferation from stem cell Embryo development in vertebrate and inverte- populations called apical meristems. The apical meribrate animals results in a nearly complete, but often stems allow the plant to continuously produce new smaller, version of the adult body. The basic body plan organs and this meristematic activity also produces is established in the embryo (or larval stages) and more meristem tissue. includes the number and position of appendages, a The root apical meristem is near the root tip; cell germ line and stem-cell populations to replenish short- division at the distal edge of this meristem produces lived tissues. Postembryonic development often root cap cells and proximal cell divisions add to a zone involves growth of the whole animal, the completion of cell proliferation next to the meristem (see Fig. 1). of the development of pre-existing organ systems In this zone of proliferation, substantial cell division such as the gonads and the maturation of functional increases the number of cells in the root; at the proxceils from stem-cell populations. The gametes dif- imal edge of this region, cells enter a zone of elongaferentiate from a population of cells which was tion in which most of the visible increase in root length typicallyset aside early in embryonic life; the presence occurs; the elongated cells then enter a zone of cell of a germ line allows irreversible somatic differentia- differentiation in which the final functional specialization in some animal tissues, such as loss of the nucleus tions of the individual cells become apparent. The (erythropoiesis in mammals), loss of chromatin pericycle, a cylindrical tissue surrounding the central (in Ascaris embryos) or nonconservative genomic core of vascular tissue in the root, is the usual source of © 1~,5, Elaevler Science lauhlisher~ B.V.. A m ~ e r c h ~ 0168 - 9S2,5/85t$02.00
prspectives
TIG -- June t 9 8 5
branch roots; root apices form from pericycle tissue, expand through the existing root tissue and emerge into the soil. Thus, the extension growth of the original root, organized by the root apical meristem, results in a continuously elongating root with an everincreasing supply of pericycle, the source of lateral roots. The shoot apical meristem provides the initial cells forming the stem and leaves of the plant. Localized cell divisions in this apex result in lateral bulges on the meristem called leaf primordia (see Fig. 2). Active apices are encased by a whorl of developing leaves, with the youngest leaves closest to the apex; the placement of the leaves, the phyllotactic pattern, is a species-specific character. On the upper side of the junction (the axil), between each leaf primordium and the stem, a new apical meristem forms concomitant with leaf initiation in most species. Thus, organogenesis in the stem is accompanied by the proliferation of apical meristems. These axillary meristems are buds, meristems which will organize a branch when growth is initiated. Each bud contains progeny of some of the original apical meristem ceils. In summary, the major features of plant development are a perpetual stem cell population (the apical meristems), repetitive production of more organs and, as a consequence of organ production, formation of more meristems. (For further information on the general principles of plant development see Ref. 1.)
Somatic sectoring in plants Fig. 1. Structure of the root tip in longn'tudinal section.
Fig. 2. Structure of the shoot tz]~of lilac ¢Syring~ in longitudinal section. A, apical merister~" AB, young axillary bud, PH, successively older leaf ~'#~rdi~,'.
Casual observation of cultivated plants shows that variegation is common during plant growth: for example, variegated ivy. Such color variegation can arise if somatic mutation occurs in one cell of the several hundred in the apical meristem (see Fig. 3) resulting in an inability to accumulate chlorophyll in progeny cells. Initially there will be a narrow sector of albino tissue on the main axis of the plant; in some branches this sector will expand because the albino cells represent a larger fraction of the cells in the axillary meristem than in the original meristem. (For information on cell lineage analysis in maize see Ref. 2 and for an overview of chimeras and cell lineage analysis in dicotyledons see Ref. 3.) Somatic changes, initially affecting just one branch on a tree, can be of great commercial importance. Many modern varieties of fruit such as the McIntosh apple and varieties of pink grapefruit were discovered as bud sports, buds producing fruit with a novel phenotype. Bud sports are propagated by grafting and are usually true to type, each graft continuing to produce the desirable fruit characteristics. In some bud sports, the novel characteristics are not transmitted in sexual crosses; sometimes the novel fruit is sterile (many apple varieties), or the bud sport may be epigenetic and the special characteristics are lost when a new embryo is formed. In other cases (such as some varieties of pink grapefruit) sexual crosses demonstrate that the bud sport resulted from a single mutation. F l o w e r formation The shoot apical meristems produce vegetative tissue until an environmental signal triggers a switch to floral development. Individual apices cease produc-
perspective
TIG - - June 1985
tion of leaf primordia, reprogram gene expression and switch to the production of the modified leaf structures that make up the flower: sepals, petals, stamens and pistils. During vegetative growth the meristem remains approximately constant in size; cell recruitment into organs is matched by cell divisions that replenish the meristem cell population in much the same way that stem cell populations in animals are maintained at a constant cell number. During floral development, however, the cells of an apical meristem differentiate into organs and no new meristems are made. Consequently, flowers terminate a stem, preventing the apical meristem from contributing further
~Anther S~amen~ ~,Filament - - ~ } 1
II~Style
Stigma1 I Pistil
(e)
(~
Zoneof mutantcells
Remainsof styleandstigma-
-
Seed
C a r p e ~ SepalsJ
'~.g (b)
Fruitwall (derivedfromovary)- ~ N (c)
Fig. 4. Structure of a completeflower (a) and the derivation of a fruit from the ovary of theflower (b and c).
Fig. 3. An apical meri,stem produces pairs of opposite leaves, each leaf derimt from about one-fourth of the apex (a). A mutant lineage (stippled area) in the meristem is represented in only one leaf of each group of four; affected leaves are all in the same rank when the plant is viewedfrom the apex. A branch arising from the axil of an affected leaf will ogntain a much larger mutant sector than the original stem, while buds in the axils of the unmarked leaoes will contain only normal d.~sue (b).
to the vegetative body. Because floral organs are more numerous and more closely spaced than are the leaves on the stem, it is likely that cell differentiation occurs more rapidly than cel/proliferation in the floral meristem. Progresswe differentiation of floral structures occurs from the base to the tip of the meristem of the floral apex (see Fig. 4). The stamen (pollen-bearing organ) and pistil (ovary-containing organ) are the most centrally located and differentiate last; in many species the gametes are drawn from a small subset of the original apical cells2.3. Thus, in plants the floral structures equivalent to the animal gonad and germ line are derived from apical meristem cells that were previously involved in organizing the somatic body of the plant. Facile reprogramming of somatic tissue into reproductive tissue must occur in plants; in annual plants most (if not all) of the apices are converted to floral structures while in perennial plants, a subset of apices are converted from vegetative to floral development leaving a residual population of buds to support the next year's vegetative growth. The most important consequence of the mode of reproduction of plants is that the gametes differentiate at the periphery of the plant from many cell lineages. Furthermore, because ax/llary buds represent a subset of the apical cells of the branch from which they arose, a single mutant apical meristem cell !n the original shoot apex can later represent an everincreasing percentage of the ceils in a branch. It is not difficult to imagine how bud sports arise on secondary or tertiary branches. The visible phenotypic changes must represent only a small fraction of the diversity of genomes present in the cell lineages forming the various flowers of a plant. With each succeeding cell division in the shoot apices of the plant, the diversity of 1 6 ~
pspectives
the lineages should increase as a result of somatic mutation, genomic rearrangements, activation of cryptic transposable elements and other means for generating genomic change.
TIG - - June 1985
such a stringent barrier, there may be great redundancy of function in plant genes such that any one function is likely to be represented by more than one gene in the haploid generation. This would mean that mutation of one allele could be compensated for by others with the same function. The high fraction of plants of recognizable polyploid origin may be particularly well buffered against gametophytic-lethal mutations. Furthermore, mutant cell lineages are in a sense tested somatically before the germ line differentiates. If a mutation in an apical meristem cell is lethal, that cell produces no somatic tissue and its progeny are not represented in the apical meristem. Mutations with little effect on cell fitness, such as albinism, will be extensively propagated in the somatic tissue before gamete formation. But a totally albino branch cannot photosynthesize and must import fixed carbon from other parts of the plant. Stewart has suggested 3 that there is extensive competition between lineages in visible chimeras; branches which grow rapidly will produce more axillary buds and can produce more flowers from the larger population of apices. Thus, some selection on the fitness of the somatic body is possible before the formation of gametes in a particular region of the plant. In some ways, a plant body is more like a population of animals than a single animal. Each apex could be considered to be a new individual which will grow and produce additional apices, in fact considerable physiologicaldata suggest that plants are composed of semiautonomous units ~. Some of the differences among individual branches may reflect genetic changes varying from gross karyotypic changes to mutations in single genes. Because plants respond to a variable environment by constant proliferation of organs differentiating in response to the environmental conditions existing at the time of organogenesis, the diversification of the apical meristems producing the somatic body of the plant may represent one of the strategies used by plants to increase the likelihood of producing appropriate organs.
D i v e r s i f i c a t i o n of the plant genome d u r i n g continuous somatic development Two important features of plants impinge on their survival after periods of genomic change: their great tolerance of karyotypic abnormalities and the existence of a haploid gametophytic generation. The influences of these two features are conflicting in terms of their impact on adaptionperse. However, the balance between them may depend on the relationship between the amount of vegetative growth involved in exploitation ofgenomic diversity in a variable environment and the success of reproduction by individual flowers. Lower reproduction efficiency would be the price pal0 for culling unfit haploid genotypes from the gametophytic generation. Considerable evidence suggests that normal development in plants is more tolerant of genetic imbalance than in animals4. For example, abnormal karyotypes are tolerated in many species, with monosomics and trisomics producing nearly normal but semisterile individuals; interspecific and intergeneric crosses often produce viable progeny. There are fewer than 100 polyploid insect species and polyploidy in vertebrates is confined to a few fish, amphibian and reptilian groups s. However, among higher plants, polyploidy is common in the ferns, occurs in about 5% of gymnosperms, 45% of dicotyledonous plants and 55% of monocotyledonous plants; polyploidization is hypothesized to result from production of unreduced gametes. The triploid and higher ploidy karyotypes which arise from sexual crosses involving unreduced gametes must be reasonably successful to be so well represented among the extant species of higher plants. An obvious question, for which we have no answer at present, is whether plant embryo development is relatively insensitive to karyotypic alterations because such changes are common and plants have evolved appropriate chromosomal and developmental controls to reduce their effects. Such tolerance might Evidence for genetic change within plants There have been few tests of the diversity of the be selected for in plants because the individual somatic lineages may diversify within the vegetative genome within a plant 4. Plants regenerated from individual resulting in gametes with a variety of tissue culture often show considerable diversity of genomic alterations. In higher animals there may be phenotype and genotype; this variation is known as great genetic diversifications within the somatic body somaclonal variation and may reflect both the prewhich affects the fitness of the individual (i.e. karyotic existing diversity of cells in the explant and additional changes in cancerous cells). However, such genomic genomic change occurring (or even induced) during diversity is not captured in the gametes and normal tissue culture. Rapid genomic change has been embryo development appears to require a normal detected between plant generations, for example in flax plants derived from parents exposed to different genome. In all plants, there is a distinct, genetically active environmental regimes s and in crosses between haploid phase of the life cycle; in higher animals there inbred lines of maize9. B. Schaal and her colleagues at are few cases of haploid cell genetic function or Washington University, St Louis, have examined the haploid cell-limited gene products. The requirement number and organization of the ribosomal genes in for independent function of the haploid gametophyte Solidago, a long-lived perennial plant, and found in plants may eliminate many lethal genes from the evidence for changes within the individual by population by selection in the haploid rather than sampling different branches (B. Schaal, personal diploid phase of the life cycle. Genetic diversification communication). Stress has been shown to induce in the somatic body may be tolerated or even adaptive cryptic transposable elements in maize ~°'~ and in the vegetative body, but lethal in the gametophyte. McClintock proposed that stress may trigger a Alternatively, because the gametophyte presents restructuring of the maize genome ~2.
TIG -- June 1985
It is possible that the developmental strategy of the plant includes the capacity to generate and tolerate diversity among the shoot apical meristems. Growth and age would both increase the likelihood of genomic changes being represented in bud sports and of genetically different offspring being produced by individual flowers. Stress may simply increase the frequency of such changes or allow more rapid selection of novel phenotypes at the somatic level, thus increasing the probability of finding genomic changes in the subsequent generation. Clearly the developmental strategy of higher plants is very different from that of higher, motile animals. Several interesting questions for research are raised by an appreciation of these differences, particularly regarding the relationship between phenotypic plasticity and change in plants and the selection and fixation of mutation in plants. Much more research will be required in order to understand the interplay between the strategy of plant development, the lack of a germ line, the constant proliferation of apical meristems, the presence of a haploid gametophytic generation and the tolerance of genomic diversity in plants.
Acknowledgements I wish to thank Paul Green for his helpful comments on plant development and Julie Wool for her assistance in preparing the manuscript. Research support was obtained from the National Institutes of Health (GM 32422).
References
perspective
1 Steeves, T. A. and Sussex, I. M. (1970) Patterns in Plant Development, 302 pp., Prentice Hall 2 Coe, E. H., Jr and Neuffer, M. G. (1978) Embryo ceils and their destinies in the corn plant. In The Clanal Basis of Development (Subtelny, S. and Sussex, I. M. eds), pp. 113-129, Academic Press 3 Stewart, R. N. (1978) Ontogeny of the primary body in chimeral forms of higher plants. In The Clonal Basis of De~lopment (Subtelny, S. and Sussex, I. M., eds), pp. 131-160, Academic Press 4 Walbot, V. and Cullis, C. A. Rapid genomic change in higher plants. Annu. Rev. Plant Physiology, in press 5 Lewis, W. H., ed. (1980) Polyploidy: Biological Relevance, Plenum Press 6 Watson, M. A. and Casper, B. B. (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Annu. Rev. EcoL Syst. 15, 233-258 7 Larkin, P. J. and Scowcroft, W. R. (1981) Somaclonal variation - a novel source of variability from cell cultures for plant improvement. Theor. Appl. Genet. 60, 197-214 8 Cullis, C. A. (1983) Environmentally induced DNA changes in plants. CRC Crit. Rev. Pl. Sc/. 1,117-131 9 Rivin, C. J. and Cullis, C. A. (1983) Modulation of repetitive DNA in the maize genome. Genetics 104, 859-860 (and unpublished data) 10 McClintock, B. (1978) Mechanisms that rapidly reorganize the genome. Stadler Genet. Syrup. 10, 25-48 11 Burr, B. and Burr, F. (1981) Transposable elements and genetic instabilities in crop plants. Stadler Genet. Syrup. 13, 115-128 12 McClintock, B. (1984) The significance of responses of the genome to challenge. Science 226, 792-801 K Walbot is at the Department of Biological Sciences, Stanford University, Stanford, CA 94305, USA.