AOBPreview originally published online on October 21, 2007
Annals of Botany 2008 101(3):319-340; doi:10.1093/aob/mcm251
INVITED REVIEW |
Determinate Root Growth and Meristem Maintenance in Angiosperms
1 Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apartado Postal 510-3, 62250, Cuernavaca, Morelos, Mexico
2 Section of Plant Biology, College of Biological Sciences, University of California, One Shields Avenue, Davis, CA 95616, USA
* For correspondence. E-mail jdubrov{at}ibt.unam.mx
Received: 9 May 2007 Returned for revision: 9 July 2007 Accepted: 17 August 2007 Published electronically: 21 October 2007
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONTERMINOLOGY AND CLASSIFICATION...CONSTITUTIVE DETERMINATE ROOT...NON-CONSTITUTIVE DETERMINATE...CELLULAR BASES OF MERISTEM...GENETIC CONTROL OF MERISTEM...DETERMINATE GROWTH, STEM CELLS...CONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Background: The difference between indeterminate and determinate growth in plants consists of the presence or absence of an active meristem in the fully developed organ. Determinate root growth implies that the root apical meristem (RAM) becomes exhausted. As a consequence, all cells in the root tip differentiate. This type of growth is widely found in roots of many angiosperm taxa and might have evolved as a developmental adaptation to water deficit (in desert Cactaceae), or low mineral content in the soil (proteoid roots in various taxa).
Scope and Conclusions: This review considers the mechanisms of determinate root growth to better understand how the RAM is maintained, how it functions, and the cellular and genetic bases of these processes. The role of the quiescent centre in RAM maintenance and exhaustion will be analysed. During root ageing, the RAM becomes smaller and its organization changes; however, it remains unknown whether every root is truly determinate in the sense that its RAM becomes exhausted before senescence. We define two types of determinate growth: constitutive where determinacy is a natural part of root development; and non-constitutive where determinacy is induced usually by an environmental factor. Determinate root growth is proposed to include two phases: the indeterminate growth phase, when the RAM continuously produces new cells; and the termination growth phase, when cell production gradually decreases and eventually ceases. Finally, new concepts regarding stem cells and a stem cell niche are discussed to help comprehend how the meristem is maintained in a broad taxonomic context.
Key words: Angiosperms, determinate root growth, indeterminate growth, meristem maintenance, quiescent centre, root apical meristem, root development, stem cells, stem cell niche
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTERMINOLOGY AND CLASSIFICATION...CONSTITUTIVE DETERMINATE ROOT...NON-CONSTITUTIVE DETERMINATE...CELLULAR BASES OF MERISTEM...GENETIC CONTROL OF MERISTEM...DETERMINATE GROWTH, STEM CELLS...CONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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In angiosperms, root and shoot growth is maintained and regulated through the activity of the apical meristems. A balance between the generation of new meristematic cells, and their transition toward differentiation, permits the maintenance of the meristem and regulates its activity. However, in many cases the meristem is genetically programmed to stop producing new cells at a specific developmental stage. In these cases, the meristem is said to be determinate (Sablowski et al., 2007). A determinate meristem usually produces a part of the plant that has a predictable size and form, such as the flower, whereas an indeterminate meristem produces parts of the plant that can grow for variable periods of time, and vary in size and shape dependent on the local environment (Sablowski et al., 2007). Thus, the indeterminacy, or determinacy, of the meristem is directly related to the type of growth of an organ. Edmund Sinnot (1960) in his book Plant Morphogenesis describes indeterminate growth this way: ‘Potentially, the plant axis can grow indefinitely in length through the activity of its apical meristem and in width through the activity of the vascular cambium. Actually, growth finally ceases for various reasons, but these axial meristems are essentially indeterminate in their activity.’ The shoot apical meristem (SAM) develops from the plumule and in turn the axial buds generate new SAMs of the shoot branches. If no transition to formation of generative organs occurs, the vegetative SAM may maintain its indeterminate growth for a long period of time. Indeterminate developmental patterns of shoot growth are underpinned by complex mechanisms involved in maintenance of the SAM (Bäurle and Laux, 2003; Veit, 2004; Barthélémy and Caraglio, 2007; Sablowski, 2007). The vegetative SAM produces leaf primordia on its flanks giving rise to determinate organs, the leaves, which take a developmental pathway for terminal differentiation. Therefore, mature leaves do not have a meristem. However, the vegetative SAM can be transformed into an inflorescence SAM, which can be either determinate, or indeterminate. Determinate inflorescence SAMs form a determinate number of flower primordia. Indeterminate inflorescences never form a terminal flower. Even when such a plant stops growing, its SAM is still present. Thus, either an inflorescence SAM in some species, or a vegetative SAM in others, can be transformed into a floral meristem that is destined to produce flower organs, and in this way to terminate its activity. These cases of floral and leaf meristems are clear examples of developmental determinacy. In the underground plant organs, clear examples are the determinate and indeterminate nitrogen-fixing root nodules of legumes. Mature determinate nodules do not have a meristem, while mature indeterminate nodules maintain a meristem (Bauer et al., 1997). Then, the fundamental difference between indeterminate and determinate organs is presence or absence of an active meristem in the mature organ.
Plant roots are surprisingly complex in their growth pattern. To the best of our knowledge, the idea of determinacy in plant roots has not been reviewed elsewhere. An analysis of determinate root growth can help us understand how the root apical meristem (RAM) is maintained and the significance of root growth patterns on the plant life cycle. We will analyse the biological significance, distribution and types of determinate root growth in various plant taxa, and the cellular and genetic mechanisms underlying the determinate developmental programme that has evolved in roots. We will establish the role of the quiescent centre (QC) in RAM maintenance, and show that root determinacy is related directly to the RAM maintenance and function.
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TERMINOLOGY AND CLASSIFICATION OF TYPES OF DETERMINATE GROWTH IN ROOTS |
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TOPABSTRACTINTRODUCTIONTERMINOLOGY AND CLASSIFICATION...CONSTITUTIVE DETERMINATE ROOT...NON-CONSTITUTIVE DETERMINATE...CELLULAR BASES OF MERISTEM...GENETIC CONTROL OF MERISTEM...DETERMINATE GROWTH, STEM CELLS...CONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Root determinacy as a general phenomenon
When seeds germinate, usually the primary root emerges before the shoot. The primary root elongates for some time and this is typically followed by emergence of either lateral or adventitious roots, leading to the development of the root system. In this paper, we will apply terms to individual roots independently of their origin: primary, lateral or adventitious. The phenomenon of root determinacy in various occasions may or may not be related to ageing of individual root axes. In general, root life span in plants is highly variable, from a few weeks to a few years (Eissenstat et al., 2000). For example, fine roots of Pinus taeda
1 mm in length can be alive up to 6 years (Matamala et al., 2003). We do not know whether these gymnosperm roots become determinate. The RAM could be lost in them during the first year, but roots stayed functional for a few more years. Thus it is important to distinguish between roots that stop growing but remain healthy and metabolically active and those that stop growing and die. Hereby, root ageing is not necessarily related to root determinacy. If the RAM remains organized, even if it is inactive, the root is not considered to be determinate. Hypothetically, roots can stop growing while their meristem is present but not active. Such cases are not well documented in angiosperms, but have been described for a gymnosperm species Libocedrus decurrens (incense cedar) roots. In this species an individual root can become dormant and then renew its growth (Wilcox, 1962), illustrating an unusual case, where a root stops growth and then resumes. As we already mentioned, the presence of the RAM, whether active or not, is the main criterion for the indeterminate condition.
In sterile root culture, the individual root axis can become inactive but roots produced from this axis can grow for many years if a subapical segment with new lateral root tips is excised and transplanted for each subsequent passage. In this way, roots can grow for many years [tomato (Solanum lycopersicon), White (1943); Convolvulus arvensis, Torrey (1958)]. This indicates that growth potential of the cultured primary or lateral root becomes lost with time in culture and these roots may appear to be determinate, but growth can be reestablished by cultivation due to activity of new lateral roots (Smirnov, 1970). This shows that root determinacy of an individual root axis and ageing of the root system are two separate processes.
Root growth is mainly studied not from a developmental but rather from an ecological perspective. Typically the behaviour and growth of the entire root mass is evaluated (Eissenstat et al., 2000; Matamala et al., 2003; Ryser, 2006), and the development of individual root axes during long periods of time is rarely studied. In this review, we will focus our attention on the developmental history of individual roots. The issue of root determinacy is considered here irrespective of the age of the whole root system of a plant, but rather as a developmental phenomenon describing individual roots. Also, in this review, although some examples of Gymnosperm roots will be mentioned, we mainly consider angiosperms. Some pteridophytes, like Azolla, also have determinate adventitious roots, and relevant information on determinate root growth in ferns can be found (Webster and MacLeod, 1996).
In pea (Pisum sativum), the growth rate of the primary root gradually increases post germination, maintains a steady state for a period of time, and then decelerates (Rost and Baum, 1988; Gladish and Rost, 1993). When grown at different temperatures ranging from 15 to 32 °C, pea seedlings reach different final root lengths as a function of temperature; roots grown at 15 °C can exceed 20 cm of final length, while roots grown at 32 °C stop growing, reaching about 12 cm of length (Gladish and Rost, 1993). The length of the RAM tends to be greatest when the rate of elongation of the primary root is at its peak, and gradually decreases until elongation stops (Rost and Baum, 1988). This decrease of growth rate is connected with differentiation events appearing closer to the root tip (e.g. Rost and Baum, 1988; Soukup et al., 2002). Other studies in cotton (Gossypium hirsutum), Arabidopsis thaliana, and several other species representing ten different families have demonstrated that the primary root eventually stops growing in all species studied (Reinhardt and Rost, 1995; Chapman, et al., 2003). Together, these observations suggest that the primary roots in seedlings of dicotyledonous plants reach a determinate length and that this final length may be dependent on the environment.
Determinacy in primary roots that is related to ageing is usually accompanied by developmental changes within the RAM. For example, RAM organization of primary roots in six species from five families was shown to change from closed type (defined in Von Guttenberg, 1960) to intermediate-open type (defined in Chapman et al., 2003; Groot et al., 2004) over a period of growth. Roots in all of these species eventually cease elongation, reaching a determinate age ranging from 14 to 41 d post-germination (Chapman et al., 2003). Similar developmental changes of the RAM organization have been well documented in Convolvulaceae (Seago and Heimsch, 1969), Asteraceae (Armstrong and Heimsch, 1976), Brassicaceae (Baum et al., 2002), and other families. For example, in A. thaliana, young roots have a closed type of RAM. As the root grows and ages, its RAM organization changes until at 4 weeks of seedling age the RAM becomes intermediate open and decreases in size (Baum et al., 2002). The number of plasmodesmata in any given cell wall within the primary RAM increases 1–2 weeks, and then decreases to a minimum by 4 weeks post-germination (Zhu et al., 1998). The number of plasmodesmata in cell walls of the root cap also decreases dramatically during this time, and cells on the periphery of the root cap undergo programmed cell death (Zhu and Rost, 2000).
In summary, all roots have their own dynamics of ageing and in this sense any root of annual, biennial or perennial plants may reach determinate length by ceasing elongation at a certain age. During this process the RAM organization changes, it becomes smaller, cells within the RAM become symplasmically isolated, and finally the RAM ceases to function. Nevertheless, for most species it remains unknown whether every root is truly determinate (which implies its RAM reaches exhaustion), or whether it can continue to perform its functions after the meristem exhaustion. We will present numerous data of well-documented determinate growth that in various developmental situations takes place either in primary or lateral roots.
Root determinacy and growth phases
The growth of most individual roots can be divided into two main phases: the phase when the growth is maintained for an undefined period here referred to as the ‘indeterminate growth phase’, and the ‘termination growth phase’ when growth eventually ceases, the determinate growth phase. During the indeterminate growth phase the RAM is continuously producing new cells. When the root reaches its determinate age, stage, and/or length, or no appropriate conditions for growth are available, the growth can be simply arrested. In this case, an organized RAM is still present and the RAM cells maintain meristematic potential. In some species, as in Libocedrus, the RAM can become dormant but later can reinitiate its function (Wilcox, 1962), or root growth can be arrested by drought, but the RAM can continue to be functional (Vartanian et al., 1994). Thus, the presence of an organized RAM at the moment of observation is evidence of potential to resume growth, and resume the indeterminate phase of the root growth. Alternatively, a developmental programme leading to complete RAM exhaustion and, differentiation of root tip cells, culminates in termination of growth. In this case, the root has ‘determinate growth’. Determinate growth can be considered ‘constitutive’ if it occurs under any environmental condition. The best examples here are the primary roots in some Cactaceae and lateral roots in plants of other families, and those in some A. thaliana mutants. Determinate growth can also be induced under some conditions, for example, phosphate starvation (Sánchez-Calderón et al., 2005). We refer to this phenomenon as ‘non-constitutive’ or ‘inducible determinate growth’.
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CONSTITUTIVE DETERMINATE ROOT GROWTH, ITS ECOPHYSIOLOGY AND ROLE |
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TOPABSTRACTINTRODUCTIONTERMINOLOGY AND CLASSIFICATION...CONSTITUTIVE DETERMINATE ROOT...NON-CONSTITUTIVE DETERMINATE...CELLULAR BASES OF MERISTEM...GENETIC CONTROL OF MERISTEM...DETERMINATE GROWTH, STEM CELLS...CONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Constitutive determinate growth is found in various taxa and represents a stable developmental programme that has certain ecological significance. However, sometimes the significance and distribution of this growth pattern within a species is obscure (Varney and McCully, 1991). For example, these authors found determinate growth in some lateral roots in the maize root system (Varney and McCully, 1991) but there is no clear understanding of a functional role of these determinate roots in maize. In this section, we further consider, in various angiosperm taxa, cases of determinate root growth which is characterized by a clear developmental scenario and ecological significance.
Determinate root growth in Cactaceae and its significance
Determinate root growth of Cactaceae was first described for lateral roots of Opuntia arenaria and O. tunicata var. davisii (Boke, 1979). In these species, plants form first-order determinate lateral roots that are a few centimetres long; their RAM is active for only a limited period of time and then these roots cease growing. New second-order lateral roots of various lengths are formed close behind the root tip. On these roots, third-order lateral roots develop, which are <1 mm in length. These show determinate root growth, and are called ‘root spurs’. The root spurs lack a root cap, the cells at their tips become differentiated and the tips become completely covered with root hairs. Spur roots may allow for an increase in root surface area, presumably increasing water uptake during infrequent rainfalls (Boke, 1979).
The determinate growth of primary roots of some Sonoran Desert Cactaceae was first reported by Dubrovsky (1997a, b). The species described belong to two subfamilies (classification by Nobel, 1988): Pachycereeae [Stenocereus thurberi, S. gummosus (Dubrovsky, 1997a, b), S. pruinosus, S. standleyi (Dubrovsky, 1999), Pachycereus pringlei (Dubrovsky and Gómez-Lomelí, 2003)] and Cactoideae [Ferocactus peninsulae (Dubrovsky, 1997b)]. A common feature of cactus roots with determinate growth is the relatively short duration of the primary root growth and early meristem exhaustion. For example, primary roots of F. peninsulae and S. gummosus grow for only 2–3 d after the start of seed germination and their final length does not exceed on average 10 mm and 9 mm, respectively (Dubrovsky, 1997a, b). After the first day of growth, the RAM length starts to decrease while RAM cells cease dividing and undergo rapid elongation and eventually differentiation. At the end of root growth, the RAM becomes exhausted and no new cells are produced, while the root tip cells elongate and differentiate. As a result of differentiation, epidermal cells form root hairs that approximate the tip of the root, and subsequently cover it completely (Fig. 1).
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The determinate developmental programme does not necessarily start very soon after seed germination. In P. pringlei, an indeterminate growth phase of the primary root is extended under optimal growth conditions and the root terminates its growth 8–9 d post-germination. In this species, water deficit accelerates the determinate developmental programme resulting in termination of growth approx. 2 d earlier (Dubrovsky and Gómez-Lomelí, 2003). We have also shown that programmed cell death is not involved in the RAM exhaustion of S. gummosus and P. pringlei, although the root-cap and root-hair cells in these species can undergo programmed cell death (Shishkova and Dubrovsky, 2005).
The common characteristic of determinate root growth in the Cactaceae, in both the primary and lateral roots, is the complete exhaustion of the RAM, coupled with differentiation of all previously meristematic cells, and loss of the root cap. This developmental programme is highly stable. Analysing thousands of plants, we have never found a case of growth reversal of the primary root from its determinate condition. Moreover, we have shown that roots regenerated from calli in tissue culture also have determinate root growth (Shishkova et al., 2007).
What evolutionary advantage may determinate root growth have in the desert Cactaceae? Rapid seedling establishment in desert environments during short optimal periods of water availability is a challenge. Successful S. gummosus seedling establishment in the Sonoran Desert is <1 % (León de la Luz and Domínguez-Cadena, 1991). The determinate root growth in such plants was proposed to present a developmental adaptation (Dubrovsky, 1998). The beginning of RAM exhaustion correlates well with the timing of lateral root initiation, and thus the loss of the functional RAM is viewed as a physiological root tip decapitation that promotes lateral root formation (Dubrovsky, 1997a, b). Some lateral roots also have determinate growth (Dubrovsky, 1997b), resulting in a compact and highly branched root system that permits efficient water and mineral uptake and transport, and facilitating rapid shoot biomass accumulation (Dubrovsky, 1998). The accumulation of shoot biomass in this case is a critical factor for plant survival in the harsh desert environment (Dubrovsky, 1996). Root determinacy in these Cactaceae species increases species fitness.
Determinate root growth in root clusters: proteoid, dauciform and other root clusters
Root clusters of several types occur both in monocotyledonous and in dicotyledonous plants. Lambers et al. (2006) use the term ‘root clusters’ to refer collectively to proteoid or cluster roots, dauciform roots, capillaroid roots and cluster-like roots.
Proteoid roots
These cluster roots consist of a large number of determinate lateral rootlets which develop on short fragments of the main root axis, giving them a ‘bottlebrush-like’ appearance. They were described in detail in Proteaceae species by Purnell (1960), and there are many papers and reviews on proteoid roots (Lamont, 1982, 2003; Dinkelaker et al., 1995; Skene, 1998; Neumann and Martinoia, 2002; Shane and Lambers, 2005; Lambers et al., 2006). Proteoid root development is almost ubiquitous in >1800 species in the Proteaceae. However, they also occur in members of seven other families: Casuarinaceae, Myricaceae, Fabaceae, Moraceae, Betulaceae, Cucurbitaceae and Eleagnaceae (Skene, 1998; Shane and Lambers, 2005, and references therein). Proteoid roots can be ‘simple’ or ‘compound’ in Hakea and Banksia species, respectively; the latter result from an assemblage of simple proteiod roots (Purnell, 1960) and are produced by only a few Proteaceae genera (Lamont, 1982). Simple cluster roots in the Proteaceae plants usually contain many more determinate rootlets per centimetre of parent root length (up to 1000!) than those in the Fabaceae (<50 rootlets per centimetre) (Dinkelaker et al., 1989; Lamont, 2003). Although very few Lupinus species produce the type of clusters that are found in L. albus (Clements et al., 1993; Bolland, 1995, 1997; Skene and James, 2000), other species of the family can produce ‘cluster-like roots’, which may function in a similar way. The rootlets of the cluster-like roots of L. angustifolius are induced on high N with an adequate P supply, and are sparser than those of the cluster roots of L. luteus. In addition, they produce fewer root hairs (Hocking and Jeffery, 2004).
Monocotyledonous families, sedges (Cyperaceae) and rushes (Restionaceae), form root clusters termed ‘dauciform’ roots and ‘capillaroid’ roots (Shane et al., 2005; Lambers et al., 2006). Cluster roots (e.g. Keerthisinghe et al., 1998) and dauciform roots (Shane et al., 2005; Playsted et al., 2006) can be also induced by P deficiency. These root clusters markedly increase the surface area of the root system and are adaptive for nutrient acquisition from impoverished soils, especially for P acquisition (Shane and Lambers, 2005; Lambers et al., 2006). Moreover, low N supply, or limited supply of K or Fe, may enhance cluster-root development in various species (Shane and Lambers, 2005). Such cluster roots are ephemeral and individual cluster roots can be physiologically active for a little more than 1 week in Lupinus albus (Watt and Evans, 1999), and perhaps 2–3 weeks in Hakea species (Dinkelaker et al., 1995). Cluster roots may show an exudative burst release of carboxylates (e.g. citrate and malate) at very high rates (Watt and Evans, 1999), but only for a few days. Carboxylate exudates are probably the most effective at mobilizing P, but cluster roots can also release other compounds; e.g. acid phosphatases (Neumann et al., 1999) may contribute significantly to P acquisition (Dinkelaker et al., 1997; Shane and Lamberts, 2005). Although cluster rootlets senesce and die, the main root axis usually remains alive and active.
The development and anatomy of the determinate proteoid rootlets of Grevillea robusta (Proteaceae) and L. albus (Fabaceae) was described by Skene et al. (1998a, b) and by Watt and Evans (1999). During differentiation of the rootlet tips, some of the epidermal cells form root hairs, which grow through the one cell-layer root cap. Eventually, the root cap is displaced by growing root hairs. In the RAM of mature rootlets, each cell layer differentiates up to its initial; the two columns of xylem elements at the rootlet apex join to form a single file of terminal xylem cells (Skene et al., 1998a). Remarkably, even the endodermis initial cells become differentiated (Skene et al., 1998b). Cluster roots of L. albus develop in a similar way (Watt and Evans, 1999). Discrete regions of closely spaced, determinate secondary rootlets emerge nearly synchronously on the same plant grown in hydroponic culture. If on day one after emergence the rootlets are almost entirely meristematic, by day three, they are already approaching their final length, the RAM is no longer present, all cells are vacuolated, and epidermal cells around the tip are developing hairs. Root hairs continue to develop until day six and they accumulate around the tips of the completely differentiated rootlets (Watt and Evans, 1999).
Dauciform roots
Dauciform root clusters of sedges (Cyperaceae) were first described by Selivanov and Utemova (1969) and later by Davies et al. (1973). They were called ‘dauciform’ roots by Lamont (1974) because of their carrot-like shape. Dauciform roots often occur in groups of 20–30, ranging in length from 2 mm to 12 mm (Lamont, 1974; Shane et al., 2005), and their tips are covered with dense, long root hairs. The dauciform roots can be either determinate, with very long root hairs over the tips of the mature roots, as in Cyathochaeta avenacea, or indeterminate, with elongated non-dauciform root axes as in other Cyathochaeta species (Shane et al., 2005). To enhance P uptake, dauciform roots also release great amounts of carboxylates, as well as other compounds, during a developmentally programmed exudative burst. They function in a very similar way to proteoid roots (Playsted et al., 2006).
Capillaroid roots
Members of the monocotyledonous Restionaceae family form ‘capillaroid’ root clusters, which were also discovered and named by Lamont (1982). The name is derived from the sponge-like properties of the clumps of rootlets, which are densely covered with exceptionally long root hairs capable of holding soil water (Lamont, 1982). Little is known about their structure, development and physiology. Lamberts et al. (2006) hypothesized that the physiology and function of capillaroid roots is similar to that of proteoid roots.
The types of root clusters considered above are usually those found on nutrient-poor soils. These short-lived roots can apparently be developed in cohorts, and increase root turnover. So, determinate growth in these roots could be an adaptation that regulates a rapid increase in root surface area to facilitate nutrient uptake.
Adhesive pads of adventitious roots in the climbing fig
Climbing vines, like the climbing fig (Ficus pumila; Moraceae), have developed a specialized structure, the adhesive pad, a cluster of short adventitious roots (Fig. 2A), that secrete a sticky substance permitting adherence to almost any substrate (Groot et al., 2003). This interesting structure was actually first reported by Darwin (1875) in his book on climbing plants. Groot et al. (2003) analysed the developmental anatomy of clustered adventitious roots. Clustered adventitious roots in juvenile F. pumila vines are initiated in pairs on either side of a vascular bundle at the 2nd to 3rd internodes of young stems. After root emergence through the cortex and epidermis, root hairs form, which secrete a substance that stains positively for polysaccharide and protein. Immediately after emergence, the RAM of the adventitious roots is short and wide (Fig. 2B). When the roots reach their determinate length (3–10 mm), the root cap tends to fall off, the RAM becomes exhausted, and its cells vacuolated (Fig. 2C). The adventitious roots and root hairs stick together forming the adhesive pad (Fig. 2A). If the adventitious roots fail to touch a substrate, they usually dry up; if they touch moist soil they tend to branch and change to a terrestrial form. A similar difference in the type of growth between the aerial adventitious roots and the soil-grown roots has also been observed in Monstera deliciosa (Hinchee, 1981). Auxin treatments on F. pumila adhesive pads suggested that auxin is not involved in the determinate growth of clustered adventitious roots (Groot et al., 2003). Adhesive root pads represent a specific case of determinate root growth that has evolved, presumably, as a plant adaptation that permits a vine to adhere to vertical surfaces for sun exposure to increase its photosynthetic capacity.
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Determinate root growth in roots of parasite and hemiparasite plants
There are about 3000 species of parasitic plants in 17 families, e.g. Schrophulariaceae, Cuscutaceae, Lauraceae, Viscaceae and others (Nickrent, 2002; Riopel and Timko, 1995). Although not many of them have been extensively studied, they are known to produce unusual structures called ‘haustoria’, considered to be highly modified roots (Kuijt, 1969). Haustorial roots come in two types: primary and secondary. Primary haustorial roots are formed at a root tip as a result of RAM cell differentiation (Kuijt, 1969; Weber, 1987). In the genus Striga (Scrophulariaceae), the root tip is triggered to become a haustorium by an induction process involving a haustoria-inducing factor (Riopel and Timko, 1995; Hood et al., 1998). The cells of the tip cease dividing, the root stops elongating, cortical cells near the tip enlarge, and hairs form near the tip (Riopel and Timko, 1995). This is followed by the new haustorium coming in contact with the host plant where it adheres to its surface and through a complicated developmental process penetrates the host and connects to its vascular system, particularly the xylem (Kuijt, 1969). This is a clear example of a determinate root growth where the root stops elongating, but the RAM becomes transformed into a specially modified structure for absorption and transport of nutrients. An interesting aspect of this development is that when the haustoria-inducing factor was experimentally removed from the parasitic seedling, the RAM re-initiated its activity, indicating developmental plasticity (Smith et al., 1990). Secondary haustoria can also form by localized cell divisions in the cortex of parasitic plant roots (Riopel and Timko, 1995) or stems, as in the case of Cuscuta (Fahn, 1982). Since these secondary haustoria do not originate from the root pericycle, it is debatable if they are actually roots.
Interestingly, the genus Pholisma (Lennoaceae) shows root dimorphism with long pilot roots, and short roots that tend to grow towards a host root; when in contact with a host, the RAM of the short root is quickly transformed into a penetrating haustorial organ (Kuijt, 1966). The role of plant growth regulators and development of primary haustoria have been thoroughly studied in Triphysaria versicolor (Orobanchaceae) (Tomilov et al., 2004, 2005). In various Cuscuta species, the tip of the haustorium penetrates the host plant and connects to the host vascular tissue (Parker and Riches, 1993; Riopel and Timko, 1995).
Determinate root growth in parasite and hemiparasite plants has evolved as a developmental programme that permits the formation of haustoria due to full differentiation of the RAM cells. As in other cases, this adaptation increases the species fitness.
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NON-CONSTITUTIVE DETERMINATE ROOT GROWTH |
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TOPABSTRACTINTRODUCTIONTERMINOLOGY AND CLASSIFICATION...CONSTITUTIVE DETERMINATE ROOT...NON-CONSTITUTIVE DETERMINATE...CELLULAR BASES OF MERISTEM...GENETIC CONTROL OF MERISTEM...DETERMINATE GROWTH, STEM CELLS...CONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Examples of non-constitutive determinate growth
Non-constitutive determinate root growth refers to those cases where determinate root growth is induced by some factor. The investigation of inducible determinate root growth provides an ideal means to study how RAM maintenance is controlled and how determinacy is regulated during the normal individual root life cycle.
Non-constitutive determinate growth apparently can be caused by a physical obstacle. When wheat root axis growth was impeded by an obstacle, growth stopped, root hairs covered the very tip of the root, and lateral roots were initiated closer to the main root tip (Watt et al., 2006). This example suggests that when physical restriction of cell division and elongation occurs, the affected RAM cells can switch their development toward differentiation.
The primary root of the A. thaliana maintains its growth at least for 4 (Baum et al., 2002) or 5 (Devienne-Barret et al., 2006) weeks. It can reach 47 cm in the Shahdara accession (Devienne-Barret et al., 2006) and 25 cm in the Columbia-0 accession (J. G. Dubrovsky, pers. obs.). As mentioned earlier, during the indeterminate growth phase the RAM continuously produces new cells. At later stages, the RAM becomes less functional, but we do not know how the growth is terminated under optimal growth conditions. In A. thaliana, determinate growth of the primary root can be induced by environmental factors, particularly, when plants are grown in conditions of P deficiency. In seedlings germinated on medium with only 1 µM of NaH2PO4, the number of cells in the RAM of the primary root gradually decreases until no meristematic cells can be found (Sánchez-Calderón et al., 2005). In these roots, all RAM cells differentiate (Fig. 3) and determinacy becomes irreversible. However, if seedlings are returned to medium with 1 mM of NaH2PO4 (optimal P level) at the stage when meristematic cells are still present, determinate growth can be reversible and the roots re-establish their growth.
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Similar behaviour of the RAM is found in A. thaliana grown on medium supplemented with 50 µM or 1 mM L-glutamate; glutamate inhibits mitotic activity of the RAM, and the length of the growing part of the root (RAM and elongation zone) decreases (Walch-Liu et al., 2006). This inhibitory effect is also present when L-glutamate is applied only to the root tip. Roots of 4-d-old seedlings transferred to medium with L-glutamate stop growing by day three of the treatment. If seedlings are transferred back to control medium, after treatment, about half of them are able to re-establish root growth within 24 h. However, none of the roots can recover if seedlings are returned to control medium after day four of treatment with this amino acid (Walch-Liu et al., 2006).
It was shown that in the RAM cells of A. thaliana glutamate triggered substantial and fast changes in cytosolic Ca2+, which was accompanied by a rapid transient membrane depolarization (Dennison and Spalding, 2000; Sivaguru et al., 2003). The GLUTAMATE RECEPTOR-LIKE3·3 (GLR3·3) gene of A. thaliana is a homologue of the mammalian ionotrophic glutamate receptor, and in two glr3·3 A. thaliana mutants the membrane depolarization response to glutamate was completely absent or very low (Qi et al., 2006). Nevertheless, a growth or developmental phenotype was not identified in the glr3·3 mutants. On the contrary, mutation of the OsGLR3·1 gene in rice results in a reduction in root meristem activity, a decrease in QC size, and disorder of root cap development (Li et al., 2006). Probably, in growth conditions that naturally activate the GLR3·3-dependent Ca2+-signalling mechanism, a similar phenotype could be observed in A. thaliana glr3·3 mutants.
These examples demonstrate that inducible determinate growth can be reversible at the initial steps of the treatment but becomes irreversible with more prolonged treatment. An essential factor that defines whether the growth can be re-established is the status of RAM cell exhaustion. If some meristematic cells remain during the course of the treatment, resumption of growth takes place.
Determinate root growth induced by fungi
It is known that 90 % of the land plant species have associations with fungi called mycorrhizae. This symbiosis involves about 6000 species of fungi and about 240 000 species of plants (Bonfante, 2003). The fungus provides the plant with nutrients from the surrounding soil, and the plant provides the fungus with sugars and other compounds (Mauseth, 1988; Phillips and Fahey, 2006). There are two types of mycorrhizae: endomycorrhizae and ectomycorrihzae. Endomycorrhizae are the most common type, found in 80 % of the vascular plants. They involve intracellular penetration of the fungal hyphae into the cell walls of epidermal and cortical cells, and formation of branched hyphal structures in root tissues (Hacskaylo, 1957; Lambais, 2006). Ectomycorrhizae are found in Betulaceae, Fagaceae, Pinaceae, Myrtaceae, and a few other families, only in trees and shrubs (Mauseth, 1988; Burgess et al., 1994).
The infecting fungal hyphae generally do not invade the RAM or the vascular cylinder (Hacsakaylo, 1957), but the roots do cease their growth soon after colonization. Unfortunately, there are very few studies on the state of the RAM in roots infected with pathogenic or mycorrhizal fungi. In mycorrhizae roots of Ornitogalum umbellatum, some root apices become completely inactive, the meristematic activity gradually decreases, the root tip cells become vaculated and differentiated, and the root tip senesces (Berta et al., 1993). In tomato roots, the pathogenic fungus, Phytophtora nicotianae var. parasitica, induces cell cycle arrest and subsequent differentiation of the meristematic cells in the root apex of approx. 70 % of the adventitious and 30 % of the lateral roots. These changes become irreversible and finally roots stop growing and die (Fusconi et al., 1999). Interestingly, the arbuscular mycorrhizal fungus, Glomus mossae, has a protective role and prevents the tomato root tip from necrosis. This fungus colonizes tomato roots tips only up to the elongation zone, but also causes an arrest in root growth by inducing differentiation of all meristematic cells in the apex (Fusconi et al., 1999). Both, pathogenic and non-pathogenic fungi in this case induce irreversible determinate root growth, as can be judged from the differentiation or death of all RAM cells.
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CELLULAR BASES OF MERISTEM MAINTENANCE |
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TOPABSTRACTINTRODUCTIONTERMINOLOGY AND CLASSIFICATION...CONSTITUTIVE DETERMINATE ROOT...NON-CONSTITUTIVE DETERMINATE...CELLULAR BASES OF MERISTEM...GENETIC CONTROL OF MERISTEM...DETERMINATE GROWTH, STEM CELLS...CONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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RAM organization and function has been reviewed in detail (Clowes, 1975, 1976; Barlow, 1976a, 1994, 2002; Ivanov, 1994, 2004; Rost, 1994; Rost and Bryant, 1996; Rost et al., 1996; Groot and Rost, 2001; Jiang and Feldman, 2005). We focus here only on how the RAM is organized relative to cell proliferation and on how its organization and function is maintained.
Cell proliferation and its maintenance in the RAM
Most of the cell divisions in the RAM take place in a transverse plane (anticlinal divisions; the new cell wall is perpendicular to the nearest root surface). Few cells divide periclinally, forming cell walls parallel to the nearest root surface, and increasing the number of cell files. The cells that initiate root cell files are called ‘initial cells’. The histogen theory of Hanstein (1870) proposed that each cell file in each tissue represents a progeny of an initial cell. Using analysis of sectors marked by transposon excision from the β-glucuronidase (GUS) marker gene, Scheres et al. (1994) demonstrated the existence of relatively permanent root cell initials, independently confirming Hanstein's histogen theory.
A division of an initial cell gives rise to two cells; one maintains its identity as an initial cell, while the other, called a ‘derivative cell’, gives rise to a cell file. In A. thaliana, WS accession, and white clover (Trifolium repens ‘Ladino’), the epidermis and peripheral root cap develop in modules of cells derived from a single initial cell. The root cap/epidermis initial divides first periclinally, and then undergoes a series of anticlinal divisions to form modules of epidermal and peripheral root cap cells, always in multiples of eight. This indicates that cell division within a given module is regulated by a counting mechanism (Wenzel and Rost, 2001; Wenzel et al., 2001). By knowing the number of cells in a meristematic cell file, it is possible to estimate the number of cycles that a derivative cell passes to form a file of cells in the meristem. Using equation N = 2n, where N is the number of cells in a cell file excluding the initial cell, and n is the number of cell cycles the derivative cell passes to form a cell file (Ivanov, 1974; López-Sáez, 1975), we can find that in most species n ranges from 6 to 8 (Barlow, 1976a; Ivanov, 1974). However, in thin roots n can range from 4 to 6. For example, in primary roots of A. thaliana during their active growth phase, or primary roots of Cactaceae before their termination of growth, N varies between 15 and 42 cells in a meristematic cell file (Fujie et al., 1993a; Dubrovsky, 1997a, b; Dubrovsky et al., 2000; Kidner et al., 2000; Sabatini et al., 2003). In these examples, the similar value of n in both root types indicates that the number of cycles within the RAM is not decisive to define a growth pattern. After a cell derivative from an initial passes n division cycles, its progeny starts leaving the meristem by displacement to the elongation zone (Fig. 4). RAM length can vary during root ontogenesis. For example, an increase in the RAM length can be a result of later transition of meristematic cells to elongation, while the pace of the division of initial cells can be maintained. Theoretically, this can happen either because cycle time of all meristematic cells is increased, or because all cells pass through additional rounds of division within the RAM.
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The organization of cell proliferation in the RAM (Ivanov, 1974, 1994; Barlow, 1976a) implies that the distal cells of the cell files are initial cells for various tissues, also called ‘functional initials’ (Barlow, 1997). Usually, distally to the functional initials there are also cells with lower proliferation activity, called ‘structural initials’ (Barlow, 1997). Thus, the initial cells, or functional initials, are located on the periphery of the group of cells which are structural initials (Barlow, 1997). Relatively infrequent cell division of both functional and structural initials in the root was known since the observations made by of the Czech botanist Bohumil N
mec at the end of the 19th century (Barlow, 1995). However, it was only after the experiments of F. A. L. Clowes with radioactively labelled DNA precursors that this meristem portion became known as the quiescent centre (QC) (Clowes, 1956). The term was proposed by Clowes to stress the differences in cell cycle duration of cells within this distal root zone compared with more proximal root portions. Now, >50 years since the formulation of the QC concept, it is well established that most angiosperms have a QC. It was proposed that, because the QC cells divide infrequently, they accumulate fewer chromosome aberrations or other genetic lesions (Ivanov, 1974). An important function of the QC in plants is its regenerative capacity. Clowes first demonstrated that after acute X-ray irradiation of maize roots, the QC behaves differently to the rest of the meristem. After irradiation, proliferative activities of the dividing meristematic and the QC cells become reversed. The QC cells, which were originally arrested mainly in G1, remain less damaged and start active proliferation (Clowes, 1964). As a result, the QC produces a new RAM, replacing the damaged one. Similar behaviour of the QC is found under other unfavourable growth conditions. At low temperature, the maize RAM becomes dormant. After transfer to optimal growth temperature, the QC cells become active and roots recover from dormancy (Clowes and Stewart, 1967; Clowes and Wadekar, 1989; Kerk and Feldman, 1994). Another type of recovery, from carbohydrate starvation, was shown in excised primary roots of maize cultured in medium lacking sucrose (Webster and Langenauer, 1973). Under these starvation conditions, neither mitosis nor DNA synthesis takes place. However, when the root explants that were starved for 48 h were then transferred to medium supplemented with sucrose, all meristematic cells, including those of the QC, started DNA synthesis during the first day after the transfer. During the second day of growth in the presence of sucrose, a typical QC is detected (Webster and Langenauer, 1973). These experiments show that when sucrose becomes available after a starvation period, all meristematic cells including the QC cells start cycling. They also show that the actively proliferating cells within the meristem participate in establishment and maintenance of the QC. Thus, the described behaviour of RAM cells in response to X-ray, cold or carbohydrate starvation demonstrate that regeneration of RAM activity starts with activation of the QC. After re-establishment of normal activity of the RAM, QC cells again become quiescent and root growth resumes.
It has been proposed that the QC is a sink for auxin that maintains an oxidized QC-internal environment, which keeps the QC cells in the G1 cell cycle phase (Kerk and Feldman, 1995; Jiang et al., 2003; Jiang and Feldman 2005). Transition from G1 to S (DNA synthesis) during activation of cell division in the maize QC was shown to correlate with establishment of a less-oxidized cell status (Jiang et al., 2003). This implies that, among other things, the redox status of cells is involved in triggering division of initial cells on the periphery of the QC. In accordance with the idea that the QC is a sink of auxin, it was demonstrated that an auxin response maximum exists in the A. thaliana QC and columella initials. This maximum is instructive for tissue patterning in the root tip (Sabatini et al., 1999). In terms of progression through the cell cycle, a large QC in some plants, which can comprise close to 1000 cells, is composed of an asynchronous and heterogeneous population of cells (Clowes, 1975; Jiang and Feldman, 2005). It was shown that after 24-h incubation with tritiated thymidine, those cells within the maize QC that were labelled were predominantly located in files continuous with the cells of inner cortex and outer stele regions (Webster and Langenauer, 1974). When maize roots were incubated for 120 h, most of the QC cells became labelled and only a few cells located in the distal QC portion remained unlabelled (Dubrovsky et al., 1982). This shows that the QC is a rather dynamic structure where relatively faster cycling cells are distributed between relatively slower cycling cells, and where after a division of a structural initial a displacement of a daughter cell which becomes a functional initial may occur.
These data collectively show that the QC and the rest of the RAM are in a close interdependent relationship. As described above, QC formation requires actively dividing meristem cells in its vicinity, and the meristem above the QC depends on the activity of the functional initials. This implies that the model of meristem maintenance (see explanation in the legend to the Fig. 4) is adequate. It remains unknown what signal(s) are involved in these cell transitions.
Indeterminate growth phase and QC in Arabidopsis thaliana
A common method to identify the location and size of the QC is to incubate roots with [3H]thymidine or 5-bromo-2'-deoxyuridine (BrdU) for a period of several hours. The cycling cells around the QC incorporate the label and the non-cycling cells of the QC do not. Few studies using these techniques have been done on A. thaliana because the roots are so small. It has been proposed that the QC in this species is composed of only four cells (Dolan et al., 1993) (QC sensu Dolan et al., hereafter abbreviated as QCD). These cells are located between the provascular initial cells and the columella initials (Dolan et al., 1993; Baum et al., 2002). Clowes did not work with A. thaliana roots. However, the concept of the QC proposed by Clowes for other species implies that the QC in plants comprises both internal cells (‘structural initials’ of Barlow, see above) and initial cells (‘functional initials’ of Barlow) of the QC (Clowes, 1975, 1976). The initial cells located at the periphery of the QC (white boxes in the model on the Fig. 4) have extended cell cycle time and thus are part of the QC (Ivanov, 1974; Clowes, 1975, 1976; Barlow, 1976a, 1997). Then the QC in A. thaliana in terms of Clowes (QC sensu Clowes, hereafter abbreviated as QCC) should be defined as the cells of the intermediate layer together with neighbouring initial cells (Fig. 5B). Indeed, about 70 % of A. thaliana initial cells do not incorporate BrdU during a 24 h treatment, while the majority of the meristematic cells incorporate the label, which suggests less-frequent cell divisions of the initial cells (Fujie et al., 1993b). Independent time-lapse analysis demonstrated that incidence of mitoses in initial cells is significantly lower compared with other cells of the RAM (Campilho et al., 2006), confirming the data of Fujie et al. (1993b). That is why we prefer to consider the QC in this species as the QCC, i.e. QCD together with adjacent initial cells for all tissues except columella (Fig. 5B). Though no studies of cell cycle duration in columella initials has been done in A. thaliana, it is known that in most species the columella initials are the most rapidly dividing cells within the meristem. Hereby, they usually are not considered to be a part of the QC (Ivanov, 1974; Clowes, 1975, 1976; Ivanov and Larina, 1976) and that is why we exclude columella initials from the QCC (Fig. 5B).
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Displacement of the initial cell derivatives into the rest of the meristem was shown by clonal analysis (Dolan et al., 1994; Scheres et al., 1994; Kidner et al., 2000). For example, using heat-shock inducible excision of the Dc transposable element, it was demonstrated that cell derivatives from the QCC can replace columella and procambium initials (including pericycle), and possibly initials of other tissues (Kidner et al., 2000). These authors estimated that initial cells for lateral-root cap and epidermis are displaced every 13 d. These data are in a good agreement with anatomical observations in A. thaliana showing dynamic changes in the RAM organization (Baum et al., 2002). Also, they confirm extended duration of the cell cycle in initial cells.
Overall, the dynamic nature of RAM, particularly the replacement of initial cells by derivatives of internal QCC cells and the fact that initial derivatives are displaced into the meristem, altogether demonstrate the strength of the model of meristem maintenance (Fig. 4) and show that the RAM is dependent on the QCC activity. This also implies that without the QC the RAM maintenance would be impossible. To prove it directly in roots with extensive indeterminate growth phase would be difficult. However, species having primary roots with short phase of indeterminate growth and with the termination growth phase occurring soon after germination could be useful for validation of this hypothesis.
RAM organization and RAM maintenance in roots with constitutive determinate growth
The RAM in cacti with determinate root growth is relatively small, with on average 15 and 24 cells per epidermal file in S. gummosus and F. peninsulae primary roots, respectively. The RAM cells divide relatively quickly, every 10–14 h for S. gummosus and 12–17 h for F. peninsulae (Dubrovsky et al., 1998). An evaluation of the steady-state growth period (Dubrovsky, 1997a, b) and the duration of the cell division cycle in the RAM (Dubrovsky et al., 1998) shows that during the short steady-state period, on average, only two cell division cycles occur in the RAM of these species. Assuming that meristematic activity is maintained until the meristem is exhausted, the maximum number of cell cycles in the meristem of primary roots is four in S. gummosus and five in F. peninsulae. The final length of the primary root varies significantly in these species (Dubrovsky, 1997a, b); in many seedlings the indeterminate growth phase is practically absent, and root growth becomes completed within 24 h post-germination (J. G. Dubrovsky, personal observation).
How is the RAM organized and how do these species terminate primary root growth so rapidly? The primary root in these species has an intermediate open-type RAM (Fig. 6) (Rodríquez-Rodríquez et al., 2003). We demonstrated that in the mature embryo of S. gummosus all root cell types are well developed. However, post-germination RAM initial cells have very limited or no activity (Rodríquez-Rodríquez et al., 2003). As mentioned above, only few division cycles take place within the RAM. Our analysis with BrdU incorporation into cell nuclei demonstrated that the QC in S. gummosus is not established. Thus, rapid termination of growth appears to be a direct consequence of the lack of a QC (Rodríquez-Rodríquez et al., 2003). Interestingly, in P. pringlei, a cactus species with a longer phase of indeterminate growth, the QC is established but only for 2–3 d. At later developmental stages, QC cells start cell divisions and no quiescent cells are detected. The timing of QC disappearance correlates well with the transition to the termination growth phase and exhaustion of the RAM (Rodríquez-Rodríquez et al., 2003). The uniqueness of these species in the Cactaceae is the fact that this developmental programme takes place in the primary root, which in most other plant species has a more extended indeterminate growth phase.
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A correlation between the type of growth with absence, or presence, of the QC was also shown in lateral roots of Euphorbia esula. In this species, short lateral roots with limited growth do not develop QC whereas long lateral roots do (Raju et al., 1964). Laser ablation experiments in A. thaliana demonstrated that QCD cells maintain the undifferentiated state of the adjacent cells (van den Berg et al., 1997). Differentiation of neighbouring cells when a QCD cell is ablated correlates well with differentiation of all meristematic cells in cactus roots with a dominating phase of growth termination when QC is not established (Rodríquez-Rodríquez et al., 2003).
Changes in RAM organization during meristem exhaustion in roots with inducible determinate growth
Little research has been published on what leads to RAM exhaustion in determinate roots (Chapman et al., 2003). Under conditions of P deficit, the RAM in A. thaliana becomes exhausted within 14 d after germination. During this process, the number of cells in the elongation zone gradually decreases from 8 to 0 by day 12. The number of meristematic cells in the epidermis decreases steadily from 25 to 0 by day 14 (Sánchez-Calderón et al., 2005), indicating that meristem exhaustion is a relatively rapid process in these conditions.
It has been shown that when cell division in the RAM is arrested, approximately half of the cells are leaving the meristem during a time period equal to the average cell cycle time in the RAM (Ivanov, 1981, 1994, 1997; Ivanov and Bystrova, 2006). If we assume the average cycle time in the A. thaliana RAM to be 16 h [from Beemster and Baskin (1998) and Dubrovsky et al. (2000)], and if cell division is arrested at the beginning of meristem exhaustion induced by P deficiency, then complete meristem exhaustion should theoretically occur in approx. 85 h (3·5 d). When experimentally determined, this period is extended to 14 d in A. thaliana (Sánchez-Calderón et al., 2005). This demonstrates that during induced determinate growth, meristematic cells continue their proliferation. Indeed, analysing transgenic plants expressing CycB1;1::GUS, a marker for meristem activity, it was shown that proliferation in the RAM at P-deficit conditions is maintained up to day 8 (Sánchez-Calderón et al., 2005). Interestingly, a QC-specific marker QC46:GUS (Sabatini et al., 1999) was detected in the RAM of plants under the same conditions up to day 10 (Sánchez-Calderón et al., 2005). This indicates that a correlation exists between the presence of cells with QCD identity and the maintenance of cell proliferation in the RAM. Remarkably, in S. gummosus, a species with constitutive determinate root growth, a decrease in meristematic activity within the RAM during meristem exhaustion is also a gradual process (Dubrovsky, 1997a), even though in this species the QC is not established (Rodríguez-Rodríguez et al., 2003).
There are a number of open questions in our understanding of the cellular bases of non-constitutive determinate growth. What is the impact of the QC in this type of growth? What cells are first targets of signals that lead to determinate growth? What is the interaction between the cells of the QC and those of the rest of the meristem? Further studies in these directions are needed to uncover the mechanisms of induced determinate root growth.
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GENETIC CONTROL OF MERISTEM MAINTENANCE AND DETERMINATE ROOT GROWTH |
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TOPABSTRACTINTRODUCTIONTERMINOLOGY AND CLASSIFICATION...CONSTITUTIVE DETERMINATE ROOT...NON-CONSTITUTIVE DETERMINATE...CELLULAR BASES OF MERISTEM...GENETIC CONTROL OF MERISTEM...DETERMINATE GROWTH, STEM CELLS...CONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Molecular mechanisms of RAM maintenance and determinate root growth in plants involve complex regulatory networks which are not well understood. The study of plant mutants that show features of root meristem exhaustion can help us understand the genetic control of RAM maintenance and determinate root growth. Determinate root growth can also be induced as a result of overexpression of certain genes. Although ectopic expression is not necessarily evidence of the importance of a specific gene for a particular process, it can help reveal the molecular players and underlying mechanisms involved. Instances where gene overexpression leads to RAM exhaustion will be considered here. The majority of mutants in which the RAM becomes exhausted are reported for the sole species, A. thaliana. Therefore, in this section we refer to A. thaliana mutants if not otherwise stated and under the term QC we mean QCD.
Four transcription factors have been found to be important for QC specification and initial cell activity. Two of them, PLETHORA1 (PLT1) and PLT2 belong to the