JXB Advance Access originally published online on January 31, 2006
Journal of Experimental Botany 2006 57(4):815-826; doi:10.1093/jxb/erj059
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
RESEARCH PAPER |
How periodic growth pattern and source/sink relations affect root growth in oak tree seedlings
INRA, Unité Plantes et Systèmes de culture Horticoles (PSH), Domaine St-Paul, site Agroparc, F-84914 Avignon Cedex 9, France
* To whom correspondence should be addressed. E-mail: Loic.Pages{at}avignon.inra.fr
Received 7 June 2005; Accepted 17 November 2005
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Seedlings of Quercus pubescens were grown in root boxes to study the growth pattern of the root system in relation to shoot development. Shoot growth was typically rhythmic. Root elongation was also periodic, in contrast to several previous reports on other Quercus species. Both taproot and lateral root elongation were depressed during expansion of the second leaf flush, with a more pronounced response of lateral root growth. Apical diameter of the taproot followed comparable but less prominent trends than taproot elongation. Modifying source/sink relationships through various defoliation treatments altered the root growth pattern. Ablation of source organs (mature leaves or cotyledons) amplified the decrease in root growth concomitant with leaf expansion. Root growth recovery was even more difficult when both cotyledons and mature leaves had been removed. Ablation of sink aerial organs (young leaves) initially suppressed competition for growth between the shoot and the root, and then caused a gradual decrease in lateral root growth. Antagonism between maximum leaf expansion and root growth reduction during the second flush, and various responses of seedlings with modified source/sink relationships, raise an hypothesis of mutual competition for carbohydrates. The gradual decrease in lateral root growth after ablation of young leaves suggests a long-term carbohydrate limitation, or auxin limitation as auxin sources have been removed.
Key words: Ablation, apical diameter, defoliation, lateral roots, Quercus pubescens, rhythmic growth, root box, taproot
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The influence of many environmental factors on the development of individual organs, including roots, have been widely characterized (Malamy, 2005
). For instance, temperature (Pritchard et al., 1990), mechanical constraints such as soil compaction (Bengough and Young, 1993), water deficit (Van der Weele et al., 2000), or local nutrient availability (Drew and Saker, 1975; Zhang and Forde, 2000) have been linked to changes in root elongation.
However, the different parts of a plant do not grow independently. Developmental responses of an organ depend not only on local conditions, but also on the environment encountered by other distant organs and on the source/sink relationships in the plant (Champagnat et al., 1986b; Gersani and Sachs, 1992; Pagès, 2000; Forde and Lorenzo, 2001). For instance, deflecting, slowing or blocking taproot growth induces various changes in lateral root growth (Riedacker et al., 1982; Thaler and Pagès, 1997). Compensatory growth of roots in response to a localized supply of nitrate or other nutrients (Drew and Saker, 1975, 1978) has been interpreted as communication between several pathways such as a systemic response to the nutrient status of the plant, and signalling by various molecules such as 
or hormones (Zhang and Forde, 2000; Forde and Lorenzo, 2001). Plants are complex integrated systems in which organs interact via various nutritional and signalling pathways (hormones, sugar, ). Communication at various distances between organs is essential to explain several major phenomena, in particular, those involved in architectural plasticity like compensatory growth, apical dominance, bud dormancy, response to defoliation or rhythmic growth of the shoot system.
Shoot rhythmic growth is a major trait of many tropical and temperate trees (Hallé and Oldemann, 1970). Rapid stem extension and leaf expansion alternate with periods of terminal bud development, with no shoot elongation or leaf emergence until a new cycle (flush) of growth begins. A regular succession of flushes persists even in uniform environments with several Quercus species (Reich et al., 1980; Champagnat et al., 1986b; Alatou et al., 1989; Alaoui-Sosse, 1994) suggesting that control of rhythmic flushing is endogenous. Various hypotheses involving interactions between the tissues of the plant have been put forward to explain periodic growth. Dynamic hormonal communication between more or less distant tissues (internodes, meristem, leaves, roots) were proposed by Maillard (1987), Thaler and Pagès (1996a), but detailed mechanisms are still unclear. Competition for water between meristems and developing leaves has also been suggested (Hallé and Martin, 1968; Borchert, 1975; Reich et al., 1980). Several authors consider that competition for carbohydrates between the different sinks is responsible for periodic changes in growth rate (Alatou et al., 1989; Barnola et al., 1993; Alaoui-Sosse, 1994; Thaler and Pagès, 1996a).
Although there are numerous studies on the possible influence of these endogenous variations on the development of the shoot system, much less data is available on the root system. First of all, the very clear growth rhythm of the shoot system for various species such as oak or rubber trees contrasts with the less pronounced variations detected on the root system. A decline in overall root growth during shoot growth and leaf expansion has been demonstrated in various species like white oak (Reich et al., 1980), cacao (Vogel, 1975), or Loblolly pine (Drew and Ledig, 1980). Lastly, Thaler and Pagès (1996a) confirmed that flushes of shoot growth alternate with periods of root growth in Hevea brasiliensis. Variations in root characteristics were clearer on laterals than on the taproot. These growth variations were thought to be related to variations in carbohydrate availability at the whole plant level, allowing rapid root elongation only during periods of shoot rest. This hypothesis was reinforced by applying shading treatments at various stages (Thaler and Pagès, 1996b). In oak trees, periodic alternations of shoot and root growth is still controversial and need to be studied further. For instance, Champagnat et al. (1986b), Harmer (1990), and Pagès (1995) did not detect any synchronous variation between shoot and taproot growth.
In this context, it is important to link root growth with source/sink relations, because these relations are subjected to vary according to the shoot growth kinetics and to various constraints such as shading or defoliation. Moreover, since root growth is distributed over a large number of root tips of different positions and sizes, the individual determination of quantitative and dynamic responses of the different roots is necessary for a return to the plasticity of the whole root system architecture. To address these points, a dynamic study on Quercus pubescens is presented in which the rhythmic growth of the shoot system is characterized and its synchronization with individual root growth and apical diameter, reflecting sink strength of the root (Pagès, 1995) is analysed. Natural variations in the source/sink relationships over time, due to the rhythmic growth pattern, were combined with contrasting defoliation treatments, with the aim of modifying relations by affecting either photoassimilate availability by removing sources or sink organs, or hormonal balance by removing auxin sources. This study focuses on growth, since branching processes will be analysed later (M Willaume, L Pagès, unpublished data).
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material
Acorns of Quercus pubescens were collected on Mont Ventoux, south eastern France (44°10' N 5°17' E). They were collected from one single tree to reduce genetic variation. Only acorns around the mean weight were used. The teguments were taken off and the acorns were put in a moist mixture of peat and vermiculite (2:1) at 24 °C for 3 d to germinate.
Growth conditions in root boxes
Thirty-three plants with a taproot of at least 5 mm long were selected and planted in 11 root boxes. Root boxes were 100 or 150 cm high, 40 cm wide, and 8 mm thick (inside dimensions) PVC boxes with opaque back and sides and a transparent front pane. The root boxes were filled with a mixture of peat with a maximum grain diameter of 10 mm and vermiculite (2:1, v:v). The whole root system developed in a plane between the transparent pane and a stretched nylon mesh (30 µm). The nylon mesh allowed the supply of the nutrient solution to the root system and prevented roots from penetrating the substrate, so that the root system was entirely visible through the transparent pane (Pagès, 1992; Iijima et al., 1998). Each box was covered individually with a soft plastic sheet in order to keep the roots out of the light.
The plants were placed in a growing chamber at 24/20 °C day/night, with 70±5% relative humidity and 16 h of daylight. Photosynthetically active radiation averaged 200 µmol m–2 s–1. The plants were watered every day with a modified Hoagland nutrient solution (Goutouly and Habib, 1996; strength: 0.5) until drainage.
The development of both the shoot and root system was recorded every 2 d for at least 50 d.
Shoot development
The developmental stage of the shoot system was described according to a terminology suggested by Alatou et al. (1989) and Harmer (1990). Two further essential stages were used: (i) stage a: end of leaf expansion of first flush; and (ii) stage b: appearance of visible leaves of second flush.
The photographs were taken from above every two days with a digital camera (Nikon Coolpix SQ). Projected Leaf Area (PLA) was measured from top-sight pictures. Pruned leaves were scanned. Projected Leaf Area and total leaf area per flush were measured with image analysis software (Image J, NIH-USA). Projected Leaf Area at stage a is well correlated to the corresponding first flush total leaf area LA (Fig. 1). It was therefore used as an estimator of the total leaf area, and leaf area growth rate was calculated using this regression and PLA data. As image analysis is subject to minor errors (about 5%) and leaves tend gradually to droop, reducing the PLA, data were smoothed during non-growing periods to avoid negative estimated leaf area growth rates.
|
Root development
The emergence and growth of the taproot and all first-order lateral roots were recorded by tracing the new growth increments with waterproof coloured pens on a transparent plastic sheet placed over the front pane (Pagès, 1992
). A new colour was used for each observation date. Second-order lateral roots which appeared during the experiment were not considered. The information on the transparent sheet was digitized using in-house software. The space (coordinates of the growth segments), structure (connections), and time (observation dates) information were all recorded. The software calculated root developmental data (position of lateral root along its parent root, emergence date, length increment) from the original tracing.
To study apical diameters, macro photographs (Nikon Coolpix SQ) of each taproot apex and of around 15 apices per tree of chosen first-order lateral roots were taken every two days. Apical diameters were measured at the basal section of the apical root cone with image analysis software (Image J, NIH-USA) at a precision of 0.01 mm.
Treatments: selective defoliation
Seedlings were manually defoliated, by removing (i) no leaves (control) on nine seedlings; (ii) the mature leaves of the first flush (ML) on nine seedlings; (iii) cotyledons and mature leaves of the first flush (CML) on six seedlings; (iv) young leaves (
5 mm) appearing on the 2nd flush (YL) on nine seedlings. This defoliation was applied continuously until the end of the experiment.
Defoliation treatments were assigned in ordered fashion. Seedlings reaching stage b on the same day were shared in equal number between the different treatments. In this way there were seedlings with various development rates in each treatment.
Statistical analysis
All data manipulation was performed using R software (The R Project for Statistical Computing, 2004). Curves giving trends in plots with numerous points were calculated using the scatter plot smoothing function ‘lowess’. Kolmogorov–Smirnov tests were used to compare data in the absence of a normal distribution.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Shoot growth
Shoot growth was not synchronous between individuals. For instance, oak seedlings reached stage b between 34 d and 56 d after sowing. As a central feature of these experiments, stage b (day of defoliation) was chosen as a reference to study the growth kinetics of seedlings. Time is thereafter counted from this day.
Typical patterns of rhythmic shoot growth were observed (Fig. 2). Whereas stem elongation ended two or three days earlier, leaf area of the first flush levelled off till stage a, reaching a total area ranging from 10.5 cm2 to 50.9 cm2. Leaf area growth rate also depended on individuals. Maximum stem elongation for the second flush occurred just after stage b and preceded leaf growth. Ablation of mature leaves (ML and CML) disrupted leaf area at stage b, but establishment of the second flush followed the control. For control and seedlings whose mature leaves had been removed, leaf growth was noticeable three days after stage b; maximum leaf growth rate was variable, but occurred 8–9 d after stage b; leaf growth ended 12–13 d after stage b at the latest. Total leaf area of the second flush was quite variable (16–66.9 cm2 for control seedlings, 14.9–71 cm2 for ML seedlings, and 10.2–42.2 cm2 for CML seedlings), but was not altered by treatment (P=0.25). In YL treatment, leaf area reached a final plateau at stage a due to continuous ablation of young leaves, but defoliation was needed daily because of their continuous appearance.
|
As leaf biomass represented a large part of total shoot biomass (on average 76%), leaf growth rate was used to characterize shoot growth in order to simplify the figures.
Taproot growth
When considering individual seedlings, taproot elongation rate was relatively stable before stage b (Fig. 3a, b, c, d). Leaf area growth of the second flush slightly affected taproot growth in the control treatment. Maximum leaf area growth rate coincided with a lower elongation rate (Fig. 3a).
|
Defoliation treatments greatly modified taproot growth during the second flush. When source organs were removed (ML and CML treatments), taproot elongation rate decreased sharply during leaf growth. Minimal taproot elongation rate occurred approximately on the maximum leaf growth day, as shown in the examples (Fig. 3b, c). Seedlings whose young leaves had been removed had a slightly higher taproot elongation rate after defoliation (Fig. 3d).
Apical diameter variations followed comparable trends, but not exactly in equal proportion or timing (Fig. 3e, f, and g, h). Apical diameter had a rather stable value before stage b. Taproot apical diameter decreased substantially during the growth of the second flush when mature leaves were removed (Fig. 3f, g), but diameter decrease during leaf growth was weak in control seedlings (Fig. 3e). Taproot apical diameter increased slightly after stage b on seedlings without young leaves (Fig. 3h).
In spite of taking care to choose uniform seedlings, growth rates differed greatly from one individual to another. Taproot elongation rate ranged from 2.3 mm d–1 to 25.4 mm d–1 (on average 15±4 mm d–1), and apical diameter from 0.69 mm to 2.05 mm (1.29±0.2 mm) during the first flush development and rest (before stage b).
As taproot elongation rate and diameter were in a fairly steady state during first flush rest (stage a to b), and the shoot showed only minor growth, mean taproot elongation and mean apical diameter between stage a and b were used to account for individual early growth variations. Taproot elongation was therefore standardized and expressed as a percentage of the mean elongation rate of the corresponding seedling during this period (Fig. 4a, b, c, d). The same principles were used to calculate standardized apical diameter for taproots (Fig. 4e, f, g, h).
|
Comparisons of the data on all seedlings confirm and complete observations on individuals. Taproot elongation rate in control seedlings began to decrease around 2 d after stage b. Elongation rates were, on average, 4 mm and 25% lower 7–12 d after stage b, but up to 50% lower for some individuals (Fig. 4a). Growth rate recovered to a great extent after leaf expansion of the second flush. The small increase in apical diameter over time was disturbed at the same time. However, the concomitant decrease was less for apical diameter (around 10%, Fig. 4e) and recovery was enhanced. To understand the relative kinetics of taproot growth and apical diameter, mean standardized taproot elongation rate versus mean standardized taproot apical diameter were compared at different times from stage b (Fig. 5a). The mean apical diameter and elongation rate did not vary significantly between period 0, 1, and 2 (–5 to 7 d from stage b) in control seedlings. However, both diameter and elongation rate values were lower in period 3 (7–12 d from stage b) than in previous steady periods (Kolmogorov-Smirnov test, P <0.01), in agreement with Figs 4a and e. In the last period studied (period 4, more than 12 d from stage b), the mean elongation rate increased, but did not reach the value found in the early stages, whereas mean apical diameter was higher than in all previous periods (Kolmogorov-Smirnov test, P <0.01).
|
Ablation of source organs amplified this pattern. There are fewer data for treatment CML because fewer seedlings were available, but elongation rate was only a quarter as much and fell by 10–15 mm d–1 after defoliation (Fig. 4b), while apical diameter fell by 25% and around 0.5 mm (Fig. 4f). Taproot values rose again 10 d after defoliation. In the same way, elongation rate and diameter decreased steeply after ablation of mature leaves (ML) and during leaf expansion. Although the falling trend was general, the intensity of the response varied between individuals. The taproot elongation rate decreased by 25% and 75% (i.e. 5–15 mm d–1) and apical diameter decrease ranged from 10–40% (0.3 mm in average). Taproot elongation rate and apical diameter recovered from day 10 after stage b. Recovery was faster and more complete compared with seedlings in which both leaves and cotyledons were suppressed. The relative positions of mean standardized taproot elongation rate versus mean standardized taproot apical diameter were synchronized up and down during the different periods (Fig. 5b, c). Neither apical diameter nor elongation rate changed from the period before defoliation (0) to the period just after defoliation (1). They then decreased significantly between periods (1), (2), and (3) successively (Kolmogorov-Smirnov test, P <0.01), and reached minimal levels at period 3 (from 7–12 d after defoliation). Whereas values at period 2 are similar for both treatments with ablation of source organs, those reached between 7 d and 12 d after defoliation (period 3) were lower when both cotyledons and leaves were removed. Apical diameter and elongation rate increased again at period 4 (Kolmogorov-Smirnov test, P <0.01) but did not reach the values found before defoliation.
When young leaves were suppressed (YL), there were no difference in elongation rate (Fig. 4d) and a slight increase in apical diameter (Fig. 4h) after the beginning of the defoliation. However, the relative positions of mean standardized apical diameter and mean standardized elongation rate did not vary significantly over the observed periods.
Lateral root growth
Total lateral root growth:
Total lateral root growth represents the increase in length of all the first order laterals. For all seedlings, total growth rate of lateral roots first increased (seedling establishment) to reach a steady level from approximately stage a to stage b (Fig. 6), when new root emergence was compensated by growth ending of older laterals. Expansion of the second flush leaves coincided with lower lateral root elongation in control seedlings (Fig. 6a). Around 12 d after stage b, i.e. after the second flush leaf area establishment, lateral root elongation increased considerably. The decrease in elongation rate corresponding with the peak of leaf growth was even more striking when organs sources were removed (ML and CML treatments: Fig. 6b, c). Lateral root growth recovered only partially after second flush leaf area establishment. Lateral root elongation rate decreased slightly and gradually after stage b on seedlings without young leaves (Fig. 6d).
|
To compare several seedlings with highly variable early growth rates, lateral root growth has been expressed as a percentage of the maximal growth rate recorded before stage b (Fig. 7). After an early increase in lateral root growth rate, growth reached a steady level until stage b. Total growth rate of lateral roots decreased from apical bud break, a few days before stage b (i.e. earlier than taproots), and progressively diminished by half for 10 d after stage b in control seedlings. It then increased markedly to reach 150% of the maximum elongation rate before stage b, 25 d later. Ablation of source organs (CML and ML) amplified the decrease: 10 d after defoliation, lateral roots had all stopped growing on several seedlings. Cumulative elongation of lateral roots generally recovered from this date, but remained lower than before defoliation. When young leaves were removed, lateral root growth progressively slowed down after defoliation to reach half its former rate 25 d later.
|
Individual lateral root growth:
The general trends in total growth hid more variable responses of individual kinetics of lateral roots which appeared before stage b. Many weak lateral roots grew for too short a period to display clear temporal trends. Long and vigorous lateral roots had variable fate after stage b. Three groups were discernible (Fig. 8a) among roots which were eventually at least 3 cm long, grew for more than 4 d and were still growing notably in the 2 d preceding stage b. Some roots were not disrupted and went on growing, or slowed down progressively (group 1); others abruptly stopped growing within 2 d after stage b (group 2); some temporally stopped within 2 d after stage b and resumed growth around 10 d later (group 3).
|
In control seedlings, a majority of vigorous lateral roots kept on growing, but 30% abruptly stopped within 2 d after stage b (Fig. 8b). In seedlings whose mature leaves were removed (ML), 95% of vigorous lateral roots stopped growing after stage b and around 45% resumed growth thereafter (Fig. 8b). When both mature leaves and cotyledons were suppressed (CML), 70% of vigorous lateral roots definitely stopped growing (Fig. 8b). When young leaves were continuously suppressed (YL), 70% of lateral roots kept on growing.
Early lateral root growth:
Differences between lateral roots that grew for a short period and vigorous lateral roots that grew for more than 4 d increased the variability observed between individual lateral roots. To suppress part of this variability due to duration of growth, early lateral root growth (i.e. in the first 2 d after lateral root emergence) was studied.
Early growth of lateral roots also varied during aerial seedling development (Table 1). In the control seedlings, the mean length of 2-d-old lateral roots appearing [–12; 0] d before stage b was 20% higher than the mean of roots appearing [0; 12] d after stage b, and 7% lower than the mean of roots appearing more than 12 d after stage b. The value for lateral roots appearing [0; 12] d after stage b was missing on the CML treatment because of the small number of observations (very few lateral roots appeared during this period). When source organs were removed (CML and ML), the mean lengths of 2-d-old lateral roots appearing after stage b were at least 25% less than the mean of roots appearing before stage b. As on the control, the lowest mean of early length occurred [0; 12] d after defoliation on seedlings with removed mature leaves. By contrast, on seedlings without young leaves, the mean length of 2-d-old lateral roots appearing [–12; 0] and [0; 12] d from stage b are equal, but 25% higher than the mean of roots appearing 12 d after stage b.
|
nLateral root diameter:
Lateral root diameter measurements were highly variable. Initial diameter at emergence ranged from 0.26 to 1.19 mm. The most general pattern was a gradual decrease in lateral root diameter with root age. No relationship was detected between residual variability from this trend, and aerial rhythm or defoliation.
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Rhythmic growth of Quercus pubescens
The observed seedlings had a rhythmic development with a cycle duration of around 21 d and a time lag between stem, leaf, and root growth. Root growth was not continuous, and varied in alternation with shoot development, with a periodic depression during leaf expansion. Nevertheless, growth variations of roots were less obvious than on shoots, and differed depending on the category of root observed. Taproot growth slowed down but did not stop during maximum leaf growth, whereas the course of lateral root growth was more complex. Lateral root growth alternated on the whole more markedly with shoot development than the taproot, but the growth pattern depended on individuals. Moreover, expressions of rhythm in root systems were obscured during the first flush because the lateral roots were establishing.
Rhythmic growth in Quercus pubescens roots agrees with observations made using similar methods on Hevea brasiliensis seedlings (Thaler and Pagès, 1996a, b) or on two-year-old seedlings of Quercus alba (Reich et al., 1980). However, they differ from the conclusions drawn for Quercus robur (Lamond, 1978; Champagnat et al., 1986a; Belgrand et al., 1987; Harmer, 1990; Pagès and Serra, 1994) in spite of a similar typical rhythm of shoot growth and the close links between Quercus species. The observed differences for this trait might be due to interspecific variability in the genus Quercus, but also to differing expressions of the rhythm due to the experimental growth conditions. Champagnat et al. (1986b) reported studies of root growth in different experimental systems such as mist boxes or nutrient solution. Even in an experimental system closer to this study's conditions, using root boxes, the rhythm may have been altered by slight differences such as substrate composition, or lower temperatures and irradiance (Champagnat et al., 1986b; Belgrand et al., 1987). Differences in methods of observation might also have prevented identification of root rhythm. Some studies focused on taproots (Lamond, 1978; Harmer, 1990), that have been shown to be less responsive to the aerial rhythm in this study as well as in Hevea brasiliensis (Thaler and Pagès, 1996a). Observations of root development have not always been linked with aerial development (Belgrand et al., 1987) and were sometimes made at longer time intervals (Lamond, 1978), or for shorter periods including only the first growth flush (Pagès and Serra, 1994). A dynamic and detailed approach covering different root types and with measurements at short time intervals over a relatively long period was necessary to detect the synchronized variations between shoot and root growth. This study's results for Quercus pubescens might boost the debate on these different species.
Effects of defoliation treatments on root growth variations
Temporal variations observed on control seedlings, and modifications of root growth induced by various defoliation treatments affecting source/sink relationships can be interpreted through two non exclusive hypothesis: mutual competition for carbohydrates between root and shoot, and modification of auxin content pattern.
Synchronism between maximum leaf expansion, i.e. maximum biomass demand, and root growth diminution during the second flush on control seedlings suggest the hypothesis of mutual competition for carbohydrates. Root growth diminution was strengthened by ablation of one source of carbohydrates (ML) and was even stronger when two sources were removed (CML). On the other hand, removal of aerial carbohydrate sinks (YL) favoured root supply and allowed growth to be maintained at first. But by mid-term, YL seedlings had less aerial source (only one flush) than the control at this stage, and a large root system to sustain: lateral root growth slowed down gradually, whilst increasing markedly on intact seedlings with a second fully developed flush.
This hypothesis is in agreement with previous research suggesting the major influence of carbohydrate supply on root development. Reducing light availability decreases root elongation in sunflower, rubber seedlings, maize, and Arabidopsis (Aguirrezabal et al., 1994; Thaler and Pagès, 1996b; Muller et al., 1998; Freixes et al., 2002). Studies with ablation of shoot organs in barley (Bingham et al., 1996), or ablation of roots in pedunculate oak, barley, or rubber seedlings (Lamond et al., 1983; Farrar and Jones, 1986; Thaler and Pagès, 1997) proved that alteration of carbohydrate source/sink relationships induces modification of root development. Variation of root growth in accordance with rhythmic shoot growth of rubber seedlings has been linked to carbohydrate availability (Thaler and Pagès, 1996a). Experiments on sugar-fed roots of wheat (Bingham and Stevenson, 1993) also suggested that the elongation rate of roots responds to carbon status. Finally, variations in root growth have been precisely linked to changes in sugar contents of the corresponding roots (Farrar and Jones, 1986; Bingham and Stevenson, 1993; Muller et al., 1998; Freixes et al., 2002). The hypothesis of competition for carbohydrate is very interesting because it gives a consistent explanation for all the four treatments, i.e. spontaneous modification of carbohydrate balance through rhythmic growth (Alaoui-Sosse, 1994) artificial limitations of carbohydrate availability at two levels through mature leaves and cotyledons ablations, and continuous removal of aerial sinks through YL treatment.
However, these treatments may also have affected auxin content in the seedlings. Removal of auxin sources such as young leaves may have induced a strong limitation in auxin content. An alteration in auxin content through the inhibition of transport of auxin from shoot to root for instance has been involved in reductions in root elongation rate (Muday and Haworth, 1994; Reed et al., 1998). The gradual reduction in growth rate observed in seedlings whose young leaves were suppressed could, therefore, be due to auxin limitation after defoliation. Auxin and carbohydrate hypotheses are not exclusive, and the action of both mediators could even interact (Malamy, 2005).
Parallel responses of apical diameter and elongation rate
The concomitant decrease of taproot diameter and elongation rate was observed during leaf expansion of the second flush. Because of this experimental system (daily watering with nutrient solution, sieved substrate, daily early measurement) root diameter variability is not related to nutrient availability (Hodge, 2004), mechanical constraints (Lamond et al., 1983; Thaler and Pagès, 1997), or diurnal variations linked to moisture status (Huck et al., 1970). Parallel responses of apical diameter and elongation rate are more likely due to both assimilate availability (Thaler and Pagès, 1996b) and competition with the shoot for sugars.
Apical diameter is an estimator of meristem size (Barlow and Rathfelder, 1984). Since variations in cell production in the root apex essentially involve the size of the division zone, and not the division rate of individual cells (Muller et al., 1998), a smaller apical diameter and, subsequently, a smaller meristem may cause lower cell production. Apical diameter has, therefore, been linked to elongation rate and interpreted as an indicator of potential growth (Pagès, 1995; Lecompte et al., 2001).
Variations in apical diameter were, however, more buffered than variations in elongation rate in agreement with Pagès (1995) and Thaler and Pagès (1996b). For instance, whereas taproot elongation could fall by 75% when mature leaves were removed, the diameter response had a smaller amplitude, with a 40% decrease. While apical diameter is an indicator of cell production, elongation rate involves two major processes, cell division and cell expansion, both affected by carbohydrate availability (Muller et al., 1998). The decrease in elongation rate is a cumulative result of the concomitant alteration of both processes.
Whereas Thaler and Pagès (1996b) observed a time lag between apical diameter and elongation rate, synchronous variations were observed on a two-day scale. It would thus have been interesting to conduct a study with a smaller time step to assess synchronism and also to improve the accuracy of measurement on lateral roots, which was impaired in this study's experiments by the presence of mucilage or condensation around the apex.
Variability of response at different levels
Although the experimental system was supposed to limit plant material heterogeneity, asynchronous growth, differences of individual mean elongation rate or apical diameter during first flush (Harmer, 1990), and variable responses to defoliation illustrate high growth rate variability between individuals. Cotyledon size may explain most of the variability in the initial stages (Lamond, 1978; Reich et al., 1980). Seedlings for which both cotyledons and mature leaves were removed (CML) had the lowest values of root growth, and recovered more slowly and less completely compared with seedlings whose only mature leaves were removed, suggesting that cotyledons still provide a significant carbohydrate amount after the appearance of the second flush, even though root growth and seedling survival has been proved to be less dependent on cotyledons from the second flush in Quercus robur (Andersson, 1996; Garcia-Cebrian, 2003; Kitajima, 2003). The high variability of response intensity and recovery after ablation of mature leaves (ML) may thus be related to an unequal supply from the cotyledons, depending notably on their size.
Within a given seedling, a steeper decrease in the elongation rate in lateral roots during the second growth flush confirmed that laterals are more responsive than taproots to trophic competition, as already observed for wheat (Bingham and Stevenson, 1993), maize (Muller et al., 1998), and rubber seedlings (Thaler and Pagès, 1996a). When source organs were removed (ML and CML), most of the laterals stopped growing, whereas the taproot only slowed down. Lateral growth decrease was noticeable from budbreak, as if laterals were sensitive to competition due not only to leaf expansion but also to stem elongation. Lateral root growth of seedlings without young leaves gradually slowed down, whereas the taproot went on growing. Indeed a larger meristem and a better ability of assimilate transport suggest that the taproot has a higher sink strength and is a better competitor for assimilates than roots of higher order (Atzmon et al., 1994; Bidel et al., 2000). Lateral roots are also more sensitive than taproots to auxin availability (Muday and Haworth, 1994). Modification of hormonal balance could also be involved in the difference of root responses observed in treatment YL.
Finally, variability in elongation rate among lateral roots of the same root system (Pagès, 1995; Freixes et al., 2002) and general determinate growth (Lamond et al., 1983; Pagès, 1995) are confirmed here by the different growth patterns on control seedlings. Lateral roots of variable age, of variable initial growth and thus of variable sink strength (Atzmon et al., 1994; Bidel et al., 2000) did not react in the same way to aerial competition or defoliation: some roots slowed down, some stopped completely and some others, potentially stronger, resumed just afterward as observed on Hevea brasiliensis (Thaler and Pagès, 1996a).
To conclude, rhythmic shoot growth, by alternating relative rest periods and intensive growth periods, modifies the endogenous whole plant context, namely carbohydrate and auxin availability and, consequently, root growth characteristics. Roots were more or less affected depending on the order of the observed roots. Lateral growth was particularly sensitive to these modifications. However, whole lateral root growth also involves the branching process, influenced too by shoot rhythm or defoliation (M Willaume, L Pagès, unpublished data).
|
Acknowledgements |
|---|
We would like to thank Valérie Serra, Josiane Hostaléry, and José Fabre for technical support, Norbert Turion for providing acorns, and François Lecompte for his comments on the manuscript. This work was supported by grants from Conseil régional Provence-Alpes-Côte d'azur.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Aguirrezabal LAN, Deleens E, Tardieu F. 1994. Root elongation rate is accounted for by intercepted PPFD and source-sink relations in field and laboratory-grown sunflower. Plant, Cell and Environment 17, 443–450.[CrossRef]
Alaoui-Sosse B. 1994. Rhythmic growth and carbon allocation in Quercus robur. 1. Starch and sucrose. Plant Physiology and Biochemistry 32, 331–339.[Web of Science]
Alatou D, Barnola P, Lavarenne S, Gendraud M. 1989. Rhythmic growth characteristics of pedunculate oak. Plant Physiology and Biochemistry 27, 275–280.[Web of Science]
Andersson C. 1996. Growth of Quercus robur seedlings after experimental grazing and cotyledon removal. Acta Botanica Neerlandica 45, 85–94.[Web of Science]
Atzmon N, Reuveni O, Riov J. 1994. Lateral root formation in pine seedlings. II. The role of assimilates. Trees: Structure and Function 8, 273–277.
Barlow PW, Rathfelder EL. 1984. Correlations between the dimensions of different zones of grass root apices, and their implications for morphogenesis and differentiation in roots. Annals of Botany 53, 249–260.
Barnola P, Alatou D, Parmentier C, Vallon C. 1993. Study of the determination of endogenous rhythmic growth of young pedunculate oak by modulating light intensity. Annales des Sciences Forestieres 50, 257–272.[CrossRef][Web of Science]
Belgrand M, Dreyer E, Joannes H, Velter C, Scuiller I. 1987. A semi-automated data processing system for root growth analysis: application to a growing oak seedling. Tree Physiology 3, 393–404.
Bengough AG, Young IM. 1993. Root elongation of seedling peas through layered soil of different penetration resistances. Plant and Soil 149, 129–139.[CrossRef][Web of Science]
Bidel LPR, Pagès L, Riviere LM, Pelloux G, Lorendeau JY. 2000. MassFlowDyn I: a carbon transport and partitioning model for root system architecture. Annals of Botany 85, 869–886.
Bingham IJ, Panico A, Stevenson EA. 1996. Extension rate and respiratory activity in the growth zone of wheat roots: time-course for adjustments after defoliation. Physiologia Plantarum 98, 201–209.[CrossRef]
Bingham IJ, Stevenson EA. 1993. Control of root growth: effects of carbohydrates on the extension, branching and rate of respiration of different fractions of wheat roots. Physiologia Plantarum 88, 149–158.[CrossRef]
Borchert R. 1975. Endogenous shoot growth rhythms and indeterminate shoot growth in oak. Physiologia Plantarum 35, 152–157.[CrossRef]
Champagnat P, Barnola P, Lavarenne S. 1986a. Quelques modalités de la croissance rythmique endogène des tiges chez les végétaux ligneux. Naturalia Monspelensia HS, 279–302.
Champagnat P, Payan E, Champagnat M, Barnola P, Lavarenne S, Bertholon C. 1986b. La croissance rythmique de jeunes chênes pédonculés cultivés en conditions contrôlées et uniformes. Naturalia Monspelensia HS, 303–337.
Drew AP, Ledig FT. 1980. Episodic growth and relative shoot:root balance in loblolly pine seedlings. Annals of Botany 45, 143–148.
Drew MC, Saker LR. 1975. Nutrient supply and the growth of the seminal root system in barley. 2. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. Journal of Experimental Botany 26, 79–90.
Drew MC, Saker LR. 1978. Nutrient supply and the growth of the seminal root system in barley. 3. Compensatory increases in growth of lateral roots, and in rates of phosphate uptake, in response to a localized supply of phosphate. Journal of Experimental Botany 29, 435–451.
Farrar JF, Jones CL. 1986. Modification of respiration and carbohydrate status of barley roots by selective pruning. New Phytologist 102, 513–521.[CrossRef][Web of Science]
Forde B, Lorenzo H. 2001. The nutritional control of root development. Plant and Soil 232, 51–68.[CrossRef][Web of Science]
Freixes S, Thibaud M, Tardieu F, Muller B. 2002. Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings. Plant, Cell and Environment 25, 1357–1366.[CrossRef]
Garcia-Cebrian F. 2003. Influence of cotyledon removal on early seedling growth in Quercus robur L. Annals of Forest Science 60, 69–73.[CrossRef][Web of Science]
Gersani M, Sachs T. 1992. Development correlations between roots in heterogeneous environments. Plant, Cell and Environment 15, 463–469.[CrossRef]
Goutouly JP, Habib R. 1996. Diurnal and spatial variations in uptake capacity in peach trees. Agronomie 16, 337–345.[CrossRef][Web of Science]
Hallé F, Martin R. 1968. Etude de la croissance rythmique de l'Hévéa (Hevea brasiliensis Müll. Arg. Euphorbiacées Crotonoïdés). Andosonia, série 2 8, 475–503.
Hallé F, Oldemann RAA. 1970. Essai sur l'architecture et la dynamique de croissance des arbres tropicaux. Paris: Masson.
Harmer R. 1990. Relation of shoot growth phases in seedling oak to development of the tap root, lateral roots and fine root tips. New Phytologist 115, 23–27.[CrossRef][Web of Science]
Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162, 9–24.[CrossRef][Web of Science]
Huck MG, Klepper B, Taylor HM. 1970. Diurnal variations in root diameter. Plant Physiology 45, 529–530.
Iijima M, Oribe Y, Horibe Y, Kono Y. 1998. Time lapse analysis of root elongation rates of rice and sorghum during the day and night. Annals of Botany 81, 603–607.
Kitajima K. 2003. Impact of cotyledon and leaf removal on seedling survival in three tree species with contrasting cotyledon functions. Biotropica 35, 429–434.[Web of Science]
Lamond M. 1978. Influence des cotylédons sur la croissance et le developpement du systeme racinaire du chêne pédonculé (Q. robur). Compte-rendus du Symposium Physiologie des racines et symbioses, Nancy 6, 228–241.
Lamond M, Tavakol R, Riedacker A. 1983. Effect of blocking the tip of the taproot on root development of oak seedlings. Annales des Sciences Forestieres 40, 227–249.[CrossRef][Web of Science]
Lecompte F, Ozier-Lafontaine H, Pagès L. 2001. The relationships between static and dynamic variables in the description of root growth. Consequences for field interpretation of rooting variability. Plant and Soil 236, 19–31.[CrossRef][Web of Science]
Maillard P. 1987. Etude du développement végétatif du Terminalia superba en conditions contrôlées: mise en évidence de rythmes de croissance. Paris VI.Paris
Malamy JE. 2005. Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell and Environment 28, 67–77.[CrossRef][Medline]
Muday GK, Haworth P. 1994. Tomato root growth, gravitropism, and lateral development: correlation with auxin transport. Plant Physiology and Biochemistry (Paris) 32, 193–203.
Muller B, Stosser M, Tardieu F. 1998. Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots. Plant, Cell and Environment 21, 149–158.[CrossRef]
Pagès L. 1992. Transparent mini-rhizotrons for studying the root system of young plants. Use for characterizing root development in young oaks (Quercus robur). Canadian Journal of Botany 70, 1840–1847.[CrossRef]
Pagès L. 1995. Growth patterns of the lateral roots of young oak (Quercus robur) tree seedlings. Relationship with apical diameter. New Phytologist 130, 503–509.[CrossRef][Web of Science]
Pagès L. 2000. How to include organ interactions in models of the root system architecture? The concept of endogenous environment. Annals of Forest Science 57, 535–541.[CrossRef][Web of Science]
Pagès L, Serra V. 1994. Growth and branching of the taproot of young oak trees: a dynamic study. Journal of Experimental Botany 45, 1327–1334.
Pritchard J, Barlow PW, Adam JS, Tamos AD. 1990. Biophysics of the inhibition of the growth of maize roots by lowered temperature. Plant Physiology 93, 222–230.
Reed RC, Brady SR, Muday GK. 1998. Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiology 118, 1369–1378.
Reich PB, Teskey RO, Johnson PS, Hinckley TM. 1980. Periodic root and shoot growth in oak. Forest Science 26, 590–598.[Web of Science]
Riedacker A, Dexheimer J, Tavakol R, Alaoui H. 1982. Experimental modifications of morphogenesis and geotropisms in the root system of young oaks. Canadian Journal of Botany 60, 765–778.[CrossRef][Web of Science]
Thaler P, Pagès L. 1996a. Periodicity in the development of the root system of young rubber trees (Hevea brasiliensis Muell. Arg.): relationship with shoot development. Plant, Cell and Environment 19, 56–64.[CrossRef]
Thaler P, Pagès L. 1996b. Root apical diameter and root elongation rate of rubber seedlings (Hevea brasiliensis) show parallel responses to photoassimilate availability. Physiologia Plantarum 97, 365–371.[CrossRef]
Thaler P, Pagès L. 1997. Competition within the root system of rubber seedlings (Hevea brasiliensis) studied by root pruning and blockage. Journal of Experimental Botany 48, 1451–1459.
Van der Weele CM, Spollen WG, Sharp RE, Baskin TI. 2000. Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. Journal of Experimental Botany 51, 1555–1562.
Vogel M. 1975. Research on the determination of the growth rhythm of the cacao tree. The Cafe Cacao 19, 265–290.
Zhang H, Forde BG. 2000. Regulation of Arabidopsis root development by nitrate availability. Journal of Experimental Botany 51, 51–59.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  M. U. Ueda, E. Mizumachi, and N. Tokuchi Allocation of nitrogen within the crown during leaf expansion in Quercus serrata saplings Tree Physiol, July 1, 2009; 29(7): 913 - 919. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||