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First published online April 28, 2006; 10.1104/pp.106.079699 Plant Physiology 141:766-775 (2006) © 2006 American Society of Plant Biologists
Phosphorus Deficiency Decreases Cell Division and Elongation in Grass Leaves1Lehrstuhl für Grünlandlehre, Technische Universität München, D–85350 Freising-Weihenstephan, Germany
Leaf growth in monocotyledons results from the flux of newly born cells out of the division zone and into the adjacent elongation-only zone, where cells reach their final length. We used a kinematic method to analyze the effect of phosphorus nutrition status on cell division and elongation parameters in the epidermis of Lolium perenne. Phosphorus deficiency reduced the leaf elongation rate by 39% due to decreases in the cell production rate (–19%) and final cell length (–20%). The former was solely due to a lower average cell division rate (0.028 versus 0.046 cell cell–1 h–1) and, thus, a lengthened average cell cycle duration (25 versus 15 h). The number of division cycles of the initial cell progeny (five to six) and, as a result, the number of meristematic cells (32–64) and division zone length were independent of phosphorus status. Accordingly, low-phosphorus cells maintained meristematic activity longer. Lack of effect of phosphorus deficiency on meristematic cell length implies that a lower division rate was matched to a lower elongation rate. Phosphorus deficiency did not affect the elongation-only zone length, thus leading to longer cell elongation duration (99 versus 75 h). However, the substantially reduced postmitotic average relative elongation rate (0.045 versus 0.064 mm mm–1 h–1) resulted in shorter mature cells. In summary, phosphorus deficiency did not affect the general controls of cell morphogenesis, but, by slowing down the rates of cell division and expansion, it slowed down its pace.
Although essential for plant growth and development, inorganic phosphorus is one of the least available nutrients in soils of many terrestrial ecosystems (Vance et al., 2003  ). Plants are profoundly affected by phosphorus deficiency because phosphorus is an indispensable constituent of nucleic acids and membrane phospholipids. Moreover, phosphorus plays a pivotal role in energy transfer, as a regulator of enzyme activity, and in signal transduction. Thus, not surprisingly, low phosphorus availability activates a series of morphological and physiological responses that maximize phosphorus acquisition (Raghothama, 1999) and are directed to maintain internal phosphorus homeostasis (Ticconi and Abel, 2004). Leaf growth depression under phosphorus deficiency is well documented (Radin and Eidenbock, 1984; Chiera et al., 2002; Assuero et al., 2004; Kavanová et al., 2006). Ultimately, this growth reduction must be due to an alteration of cell division or cell elongation parameters.
We have chosen a grass leaf system to investigate the cellular bases of growth reduction under phosphorus deficiency. In grasses, growth is confined to a short tissue segment located at the base of the developing leaf enclosed by older sheaths (Kemp, 1980
The contribution of the different cellular parameters to leaf growth reduction under nutrient stress is not well understood. Few studies addressed the effects of phosphorus deficiency and gave different results. In cotton (Gossypium hirsutum), Radin and Eidenbock (1984) concluded that reduced cell expansion underlay reduced leaf size, whereas, in soybean (Glycine max), Chiera et al. (2002) concluded that reduced cell division was the major cause. Although this divergence may be related to a different species response, it may also arise from the fact that neither of the studies directly measured these parameters. Instead, the role of cell expansion was inferred from smaller leaf cells and the role of cell division was inferred from reduced cell number. In maize (Zea mays), the first monocot studied, Assuero et al. (2004) attributed the reduction in leaf growth to a decreased cell production rate. In the only other kinematic study of phosphorus effects on leaf growth in the grass Lolium perenne, low relative elongation rates along the elongation-only zone caused a severe reduction of leaf growth (Kavanová et al., 2006). This study provides a comprehensive analysis of the cellular responses underlying reduction of the leaf elongation rate in L. perenne leaves growing under phosphorus deficiency. Using a kinematic approach, we evaluated which parameters determining the number of produced cells and their final length responded to changes in phosphorus status and which did not. This included (1) number of meristematic cells as controlled by a (constant) number of division cycles of the initial cell progeny; (2) duration of cell elongation as determined by a spatially controlled elongation-only zone length; (3) rate of cell division as determined by the growth rate of meristematic cells and a (constant) mitotic cell length; and (4) rate of mitotic and postmitotic elongation.
Leaf Elongation Rate L. perenne plants grew at low (0.02 mM) or high (1 mM) phosphorus supply. Growth at low phosphorus supply caused a 42% reduction in the phosphorus concentration in the leaf growth zone (P < 0.001; Table I ) and a 39% reduction in the leaf elongation rate (P < 0.001; Fig. 2 ). In both treatments, leaves selected for measurement elongated at a steady rate over time (Fig. 2).
The treatment effect on the leaf elongation rate was entirely due to the different phosphorus nutrition status because selected tillers of low- and high-phosphorus plants did not differ in size or developmental variables: Leaf blades and sheaths had similar lengths, and the tillers held a similar number of leaves (Table I). Further, growing leaves were in the same developmental stage, indicated by the ratio of the growing blade length to the blade length of the youngest expanded leaf (Table I). This ensured that effects of phosphorus status on growth were not confused with effects of size and development (Kavanová et al., 2006 ).
The reduction of leaf growth under low phosphorus originated partly from decreased cell proliferation in the division zone. Phosphorus deficiency reduced the cell production rate (i.e. the cell flux out of the division zone estimated from the leaf elongation rate and final cell length [Eq. 2]) by 19% (P < 0.01; Table II ).
This difference arose entirely from a different average cell division rate, that is, the number of cells produced per cell present in the division zone per unit time. Meristematic cells divided at a 39% lower rate in low-phosphorus plants (P < 0.01; Table II). As a result, the average cell cycle duration (Eq. 8) was 10 h longer in low-phosphorus plants (Table II). Phosphorus deficiency did not affect the average number of cells in a meristematic cell file (P > 0.1; Table II). Cell division was confined to the basal 0.9 ± 0.1 mm in low-phosphorus plants and to 0.6 ± 0.1 mm in high-phosphorus plants, but this difference was not statistically significant (P = 0.06). It is important to note that we did not derive the length of the division zone and the number of meristematic cells from cell deposition rates. Instead, we counted all cells present in individual meristematic cell files from the leaf base to the position of the last recently formed perpendicular cell wall. A closer examination of these data revealed that the number of cells per meristematic cell file was a weighted average of two major groups of files: files with approximately 32 cells and files with approximately 64 cells. Low- and high-phosphorus plants had a similar frequency distribution of these two groups (data not shown). The number of division cycles necessary to displace a transversal cell wall from the basal to the distal boundary of the division zone (i.e. the average number of division cycles of the progeny of a cell formed by the division of the initial cell at the base of the meristem) can be derived from the number of cells in the division zone (Eq. 10). In both phosphorus treatments, the number of division cycles was, on average, five to six (P > 0.1; Table II). Frequency distribution of the number of division cycles in different meristematic cell files revealed distinct peaks around four, five, and six, indicating that variability exists between cell files within one division zone (Fig. 3 ). Whereas in high-phosphorus plants cell files were equally distributed around five and six division cycles, low-phosphorus plants tended to have a frequency distribution shifted toward six division cycles.
As a consequence of a similar number of division cycles but longer average cell cycle duration, the average residence time of a cell in the division zone tended to be longer under phosphorus deficiency (144 ± 55 h versus 81 ± 37 h in high-phosphorus plants). Thus, cells in low-phosphorus plants tended to maintain meristematic activity for a longer period of time.
Cell length was typically constant within each individual meristematic cell file up to the position where division stopped (Fig. 4 , inset). When averaged over each treatment, average cell lengths were stable along the first half of the division zone and phosphorus deficiency did not affect this pattern (Fig. 4), but average cell length increased in the second half of the division zone by 23% in low- and 17% in high-phosphorus plants. This increase was due to the fact that in some meristematic cell files the number of division cycles of the initial cell progeny was five (meristem length approximately 32 cells), whereas in others it was six (meristem length approximately 64 cells). Hence, in the second half of the meristem, dividing cells (maintaining their average length unaltered) coexisted with nondividing cells (that were increasing in length). This is also appreciated by comparing the stability of minimal cell lengths against the increase in maximal cell lengths.
The stability of cell length along the division zone provides important information on the balance between relative rates of cell division and elongation (for discussion, see Green, 1976 ). It implies that the relative rates of meristematic cell elongation were very close to the average cell division rates (0.028 ± 0.005 h–1 in low- versus 0.046 ± 0.008 h–1 in high-phosphorus plants). Phosphorus deficiency did not affect the size at which cells divided or, consequently, their length at birth: The 39% higher average cell division rate of high-phosphorus meristematic cells means they had a 39% higher relative elongation rate.
Whereas one-half of the leaf growth reduction under phosphorus stress was due to a reduced cell production rate, the other half originated from a decrease in final cell length. Mature epidermal cells were 20% shorter in low-phosphorus plants (P < 0.01; Table II; Fig. 5A ). The final length of a cell depends on three factors: the length of the cell leaving the meristem (i.e. when it enters the elongation-only zone) and the relative rate and duration of the elongation-only phase. Phosphorus deficiency affected the latter two, but cell size at the position where elongation started was not different: 24.2 ± 3.8 µm in low- versus 22.5 ± 3.4 µm in high-phosphorus plants (P > 0.1; Fig. 4).
Spatial Analysis of Postmitotic Elongation
Cell elongation was confined to the basal 31 to 36 mm of the growing leaf in low- and high-phosphorus plants, respectively (P > 0.1; Fig. 5A). The number of cells in the elongation-only zone was also not affected by phosphorus deficiency (136 ± 9 in low- and 117 ± 9 in high-phosphorus plants; P > 0.1). This confirms our previous observation (Kavanová et al., 2006 Relative elongation rates along the elongation-only zone obtained by differentiating displacement velocity profiles (Fig. 5B) were uniformly lower at all positions in low-phosphorus plants (Fig. 5C). Thus, phosphorus deficiency did not modify the spatial distribution of relative elongation rates, which were, on average, 30% lower in low-phosphorus plants (P < 0.05; Table II).
Furthermore, we carried out a temporal analysis of the elongation of an individual cell from the moment it enters the elongation-only zone. The spatial profiles of cell length, displacement velocity, and relative elongation rate were transformed into time courses using the growth trajectory function, which relates spatial position of a cell to time coordinates (Eq. 5). This analysis revealed that cells expanded for a substantially shorter period in high-phosphorus plants (P < 0.05; Table II) because they moved more rapidly through the elongation-only zone. Thus, the higher relative elongation rate of high-phosphorus plants was partially offset by a shorter elongation duration (Fig. 6 ).
Growth regulation constitutes a major field of interest in plant physiology. However, the cellular bases of growth reduction under stress conditions are not fully understood. This kinematic study showed that, under phosphorus deficiency, the reduction of leaf growth in the grass L. perenne arose from inhibition of cell division and elongation rates, leading to reductions in both the cell production rate and the final cell length. The lengthened average cell cycle duration in low-phosphorus plants was linked to a slower elongation rate so that meristematic cell length was not modified. Notably, other variables were unrelated to phosphorus status. In the division zone, phosphorus deficiency did not affect the number of division cycles (of the progeny of a cell formed by the division of the initial cell at the base of the meristem). In the elongation-only zone, phosphorus deficiency did not modify the position where postmitotic elongation stopped. Hence, phosphorus deficiency did not affect the putative controls of the cell morphogenetic program, but, by slowing down the rates of cell division and elongation (and thus increasing the residence time in both zones), it slowed down the pace at which it was carried out.
Coupling between cell elongation and cell division has been observed under undisturbed conditions in plant meristems, where cells double in size from birth until the next division (Cánovas et al., 1990 Our study shows that phosphorus deficiency decreased the average division rate of meristematic cells. But phosphorus deficiency did not affect meristematic cell length (Fig. 4), implying that a decrease in the division rate was accompanied by an equivalent reduction in the elongation rate. Therefore, phosphorus deficiency did not affect the close coordination between cell growth and cell division in the leaf meristem (see Fig. 7 , trajectory A).
What would be the result of uncoupling cell division from elongation in the meristem? Figure 7 illustrates the possible outcomes. A factor that decreases cell division rate but does not affect elongation will increase meristematic cell length (Fig. 7, trajectory B). This would also increase the initial length at which cells start expanding, and result in longer mature cells, even though their elongation rate is not affected. The same will occur when a factor increases the elongation rate but does not affect the division rate (Fig. 7, trajectory C). This analysis also illustrates the risks of inferring changes in cell division or elongation rates based only on meristematic or mature cell length.
The coupling of cell growth and division in proliferating cells may be achieved by alternative means: The cell division rate may affect the cell growth rate, the cell growth rate may influence the cell division rate, or both processes may respond to a common signal. In the first scenario, phosphorus deficiency would have inhibited cell cycle progression, and the reduced cell division rate would have decreased the cell elongation rate. Some authors have indeed suggested that cell division might affect cell growth (Doerner et al., 1996
The second scenario puts forward that a lower elongation rate of meristematic cells lengthened the average cell cycle duration. This view is supported by the fact that the probability of G1-to-S transition, a major cell size checkpoint, increased with increasing cell size (Cánovas et al., 1990
It is not clear which signal could regulate both cell growth and division rate in the third scenario. Cytokinins are a putative candidate because phosphorus deficiency decreases their shoot levels (Horgan and Wareing, 1980
A decrease in the relative elongation rate along the elongation-only zone led to shorter mature epidermal cells in phosphorus-deficient plants and thus contributed to a decrease in the leaf elongation rate (Fig. 5). Other parameters influencing final cell length were little affected by phosphorus status (the length of cells leaving the division zone; Fig. 4) or even increased under phosphorus stress (elongation duration; Table II).
Proliferating cells grow primarily by an increase in the cytoplasmic volume, whereas cells in the postmitotic phase expand primarily through an increase in the vacuolar volume (Fagerberg, 1984
Whereas division and elongation rates varied in response to phosphorus status, the size of the division and elongation-only zones remained unaffected. Two main models of growth zone regulation have been proposed for roots and may also be valid for grass leaves. The first one proposes that a spatial gradient of growth regulators determines the developmental state of cells at any position along the growth zone (Barlow, 1984 We evaluated whether the length of the cell division zone could be determined by a temporally limited proliferation of meristematic cells. Under low phosphorus, cells were proliferative for a longer time than under high phosphorus, suggesting either that the termination of cell proliferation was not time regulated or that the temporal control changed. The spatial dimensions of the division zone might be related to the constant number of division cycles of the progeny of a cell formed by the division of the initial cell at the base of the meristem. Regardless of phosphorus status, the number of division cycles before cells entered into the elongation-only zone was four to six. There was more variation between cell files within a division zone than between plants of different phosphorus status, showing the importance of evaluating meristem parameters for individual cell files.
A review of the literature provided further support for the observed constancy. The length of the division zone in leaves of different C3 grass species has been reported to vary between 1 and 8 mm (Beemster et al., 1996
Interestingly, this study indicated that the length of the elongation-only zone was not affected by phosphorus deficiency. As discussed previously, phosphorus deficiency decreased the flux of cells through this zone but did not affect the elongation-only zone length, thus increasing the duration of an individual cell's elongation. This contradicts the view that the termination of cell elongation is time regulated. Support for the temporal regulation has been obtained by finding the opposite; namely, that the size of the elongation-only zone is proportional to the number of cells flowing through it (i.e. cell production rate) because each cell has a temporal program of elongation to execute (Beemster and Baskin, 1998
In contrast to the only other kinematic study of phosphorus effects on leaf growth (Assuero et al., 2004
Plant Material and Growth Conditions Surface-sterilized seeds of Lolium perenne L. cv Condesa were sown in pots (diameter 5 cm, height 35 cm) on a mixture of quartz sand with 63 mg phosphorus per pot in the form of finely ground Hyperphos (Deutsche HyperPhos-Gesellschaft), providing a source of phosphorus with low availability. Each pot contained one plant. Plants grew in a growth chamber (E15; Conviron), with 20°C (day)/15°C (night), 70% relative air humidity, and 525 µmol m–2 s–1 photosynthetic photon flux density at plant height for 16 h/d. Plants were irrigated for 21 d after sowing four times a day with 25 mL of modified one-half-strength Hoagland solution [0.02 mM KH2PO4, 2.5 mM KNO3, 2.5 mM Ca(NO3)2, 1 mM MgSO4, 0.5 mM KCl, 0.5 mM NaCl, 0.125 mM Fe-EDTA, 23 µM H3BO3, 4.5 µM MnSO4, 0.38 µM ZnSO4, 0.16 µM CuSO4, and 0.05 µM Na2MoO4]. Thereafter, two levels of soluble phosphorus were applied: 0.02 mM KH2PO4 (low phosphorus) and 1 mM KH2PO4 (high phosphorus).
To avoid confounding phosphorus status with tiller size effects (see Kavanová et al., 2006
In five to six plants per treatment, representative tillers with at least three fully expanded leaves were selected at each date. The leaf elongation rate was determined on the youngest, most rapidly growing blade during the phase of maximal growth, when the leaf elongation rate was near constant. During this developmental stage, leaf growth is due exclusively to the activity of the blade growth zone, and cell division in the blade meristem and blade expansion are approximately steady (developmental stage A
Twelve plants per treatment were sampled at the end of the light period 49 d after sowing in high- and 63 d after sowing in low-phosphorus plants. Leaf growth zones were dissected from leaves similar to those used for leaf elongation rate measurements. Fresh weight was recorded, samples were frozen in liquid N2, freeze-dried, weighed, ground, and stored at –25°C. Phosphorus concentration was determined on 10- to 20-mg pooled samples as described by Kavanová et al. (2006)
The growing blade was carefully freed from surrounding older leaves in six plants per treatment 47 d after sowing in high- and 61 d after sowing in low-phosphorus plants. A transparent replica of the abaxial epidermis along the basal 50 mm of the growing leaf was taken as described by Schnyder et al. (1990)
Images were captured using a digital camera (Camedia C-5050Z; Olympus) fitted to an optical microscope (Olympus BX50). Leaves were excluded if the ligule was situated more than 1 mm from the leaf insertion to ensure that only the blade growth zone was contributing to the leaf elongation (Schnyder et al., 1990 In addition, a sequence of overlapping images was taken along the basal 2 mm (starting from the ligule), and composite images were created. The length and distance from the leaf base of every cell in eight to 12 cell files located midway between files containing stomata were recorded in each leaf. Mean epidermal cell length over 50-µm intervals was determined for each plant and then averaged over plants of the same treatment. Similarly, the length of the longest and shortest epidermal cell over 50-µm intervals was determined for each plant and then averaged over plants of the same treatment. In each cell file, we recorded the most distal position of a newly formed (visually thinner) perpendicular cell wall, which was used as a marker for the distal end of the cell division zone.
This is a novel method based on the same rationale as that introduced by Beemster et al. (1996)
Analysis of Cell Elongation
Final cell length (Lf, mm) and leaf growth zone length (LLGZ, mm) were determined by fitting a Richards function (Morris and Silk, 1992
Cell flux (F, cells h–1), the rate at which cells are displaced past a particular position, was estimated at the distal end of the elongation-only zone from the leaf elongation rate (LER) and final cell length (Lf):
).
In the elongation-only zone, the displacement velocity of a cell at a certain position is the result of the elongation of all cells located more basally in the growth zone. Therefore, displacement velocity increases with distance from the leaf base and finally becomes constant and equal to the leaf elongation rate. Under steady-state growth, there is strict correspondence between local cell length [L(x), mm] and local displacement velocity [v(x), mm h–1] in the elongation-only zone (Morris and Silk, 1992
The relative elongation rate in the elongation-only zone (Re, mm mm–1 h–1; synonymous terms that have been used before are strain rate, relative elemental growth rate, and segmental elongation rate) was estimated by differentiating numerically the displacement velocity with respect to position. This parameter provides a measure to compare the magnitude of the elongation rate independently from the absolute cell length at a given position (Silk, 1992
The average relative elongation rate in the elongation-only zone (
The spatial profiles of cell length, displacement velocity, and relative elongation rate were transformed in temporal profiles by calculating the trajectory function that describes the time it takes for a cell located at position x to be displaced to the end of the elongation-only zone (Silk et al., 1989
The average elongation duration (i.e. the residence time of a cell in the elongation-only zone; Te, h) was then calculated as:
The average division rate of cells in the meristem can be determined by relating the cell production rate to the number of cells per meristematic cell file in the division zone (Ivanov and Dubrovsky, 1997
The average cell division rate (D, cell cell–1 h–1) was calculated as:
; Ivanov and Dubrovsky, 1997). The number of cells in a meristematic cell file (Ndiv) was directly counted from the basal end of the division zone (i.e. the ligule) to the position of the last recently formed perpendicular cell wall. Meristematic cell length was determined as the average cell length between the basal and the distal end of the cell division zone.
The average cell cycle duration (Tc, h), the time from a cell's formation to the next cytokinesis that yields two daughter cells, was calculated as follows (Green, 1976
; Beemster and Baskin, 1998):
The average number of division cycles of the progeny of a cell formed by the division of the initial cell at the base of the meristem (i.e. the number of division cycles necessary to displace a transversal cell wall from the basal to the distal boundary of the division zone) was determined as follows (González-Fernández et al., 1968
Differences between treatments were tested by Student's t test (Statistica 6.0; Statsoft). The error associated with parameters calculated from averages (e.g. cell production and average cell division rate) was estimated by Gaussian error propagation. Results are shown as means ± SE.
The technical staff at Lehrstuhl für Grünlandlehre provided invaluable assistance, particularly Wolfgang Feneis, Anja Schmidt, and Angela Ernst-Schwärzli. We especially thank Milan Balá  (Department of Plant Physiology and Anatomy, Masaryk University, Brno, Czech Republic) and Stefan Raidl (Department Biology I, Systematic Botany and Mycology, Ludwig-Maximilians-Universität, Munich, Germany) for their hospitality and access to microscopes, and Tobias Baskin and an anonymous reviewer for valuable comments on a previous version of this manuscript. Received March 8, 2006; returned for revision April 20, 2006; accepted April 23, 2006.
1 This work was supported by the Deutsche Forschungsgemeinschaft (SFB 607).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Hans Schnyder (schnyder{at}wzw.tum.de). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.106.079699. * Corresponding author; e-mail schnyder{at}wzw.tum.de; fax 49–8161–713243.
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ABSTRACT
RESULTS
a'). The progeny of the initial cell at the base of the meristem goes through a certain number of division cycles, thus determining the number of cells per meristematic file. Upon entering the elongation-only zone (b
0.001; NS, not significant, P > 0.05.
) and low (0.02 mM, 
) phosphorus supply. The arrow indicates the time when the kinematic analysis was performed. Data are means of five to six plants on each date (±SE).
, mm mm–1 h–1) was calculated as:
-expansin from soybean. Plant Physiol 126: 244–252