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JXB Advance Access originally published online on September 5, 2005
Journal of Experimental Botany 2005 56(421):2821-2829; doi:10.1093/jxb/eri274
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© The Author [2005]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

RESEARCH PAPER

Perturbed reproductive development in salt-treated Sorghum bicolor: a consequence of modifications in regulation networks?

G. Nissim Amzallag*

The Judea Center for Research and Development, Carmel, 90404, Israel

* Fax: +972 2 9960061. E-mail: nissamz{at}bgumail.bgu.ac.il

Received 18 May 2005; Accepted 29 July 2005


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
In Sorghum bicolor, tolerance to salinity is improved by a 3-week treatment with 150 mM NaCl during early vegetative development. However, a strong decrease in fertility is also observed, suggesting that reproductive development becomes perturbed by this adaptive response to salinity. This study is an attempt to clarify the origin of such a paradoxical phenomenon. The relationships between end-cycle characters are modified by the NaCl treatment: some linkages disappear, while others are strengthened, especially those linking fertility with plant height. In parallel, a transient reduced level of linkage between leaf characters is observed around the unfolding of the eighth to the tenth leaves, defining a critical period in vegetative development separating two discrete phases. A relationship is observed between events occurring during this short critical period and the NaCl-induced perturbations in fertility. This suggests that reproductive development is conditioned by the influence of salinity on events occurring during a short period of vegetative development, independently of the level of tolerance to salinity quantified by the rate of vegetative growth.

Key words: Connectance, critical period, fertility, individuality, phenotypic plasticity, regulation networks, salinity


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Variations in tolerance to salinity throughout development have been reported for a long time (Strogonov, 1964Go (p. 13); Romero and Maranon, 1994Go; El-Saidi, 1997Go; Flowers, 2004Go). In most of the cases, the authors observed a gradual increase in tolerance from germination to flowering. In soybean, this increase in plant tolerance is not reflected at the cellular level, since a similar sensitivity to NaCl is observed in callus from germinating seedlings or late vegetative plants (Bourgeais-Chaillou et al., 1992Go). Accordingly, the phenomenon of increasing tolerance to salinity has frequently been related to a gradual improvement in root selectivity throughout development, that prevents an over-accumulation of Na and Cl ions in the shoot tissues (Romero et al., 1994Go).

However, some observations revealed the limitations of such an explanation. In some species, an abnormal ontogeny and organogenesis of reproductive development have been described independently of the NaCl effect on growth and leaf morphogenesis (Solovev, 1960Go; Dhingra and Varghese, 1993Go; Amzallag, 1998Go). Working with chickpea, Dhingra and Varghese (1997)Go noticed the following paradox: ‘the plants receiving saline irrigation prior to florogenesis are visibly healthy and sturdy, but unable to support the development of a good number of pods with healthy seeds.’ Such a perturbation in reproductive development may be alleviated by hormonal treatments (Singh and Jain, 1982Go; Dhingra and Varghese, 1997Go). This suggests that, beside a ‘poisoning effect’ of NaCl on cellular physiology, the NaCl-induced change in the hormonal balance may represent an important factor of perturbation in the expression of reproductive development. As suggested by Munns (2002)Go, tolerance to salinity appears as a complex function involving interference of many scales of organization, from the regulation of gene expression to whole plant interactions.

In Sorghum bicolor, no simple relationship between capacity of growth during vegetative development and fertility has been noted in salt-treated plants (Amzallag, 1996Go). This is particularly observed on plants exposed to salinity (150 mM NaCl) from early vegetative development (Amzallag, 1998Go). This treatment enhances the tolerance to salinity (Amzallag et al., 1993Go), suggesting that abnormal reproductive development is not directly related to a toxic effect of NaCl.

Vegetative development is not linear in grasses (Slafer and Rawson, 1994Go). Instead, it may be represented as a succession of phenophases interspaced by short critical periods during which between-organ interactions may be reset (Amzallag, 2002Go, 2004Go). In Sorghum bicolor, reproductive development is influenced by NaCl-induced changes in the regulatory network occurring during a critical period in vegetative development, around the fifth to the sixth leaves (Amzallag and Seligmann, 1998Go; Amzallag, 2001aGo, 2002Go). Thus, the abnormal decrease in fertility inherent to the salt-adaptation response may be a consequence of changes in the regulatory network related to the increase in tolerance. This study is an attempt to test such an hypothesis.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Plant material and growth conditions
Seeds of Sorghum bicolor (L.) Moench (male parent (inbred line) of the commercial F1 hybrid cv. 610) were a gift of the Hazera Seed Company (Mivhor, Israel). They were soaked overnight and sown in vermiculite moistened with tap water. Five days following imbibition, seedlings were transferred to 15 l containers filled with a modified half-strength Hoagland solution according to Amzallag (2001a)Go. Plants were grown at a density of 12 individuals per container. In salt-treated plants, NaCl was added from day 8 following imbibition by six daily increases of 25 mM NaCl in the root solution. CaCl2 was added together with NaCl in order to maintain a Ca:Na ratio of 1:30. This NaCl treatment was maintained until the end of the life cycle. Evaporation was daily compensated for by the addition of deionized water, and the root media were changed weekly from day 8 following imbibition. The experiments were performed in a greenhouse, under the natural photoperiod of June to September at Carmel, and the natural light intensity (maximum of 1200 µmol m–2 s–1 at noon). Day/night temperature of the air was about 30/15 °C, and the day/night relative humidity was about 75–85/85–95%. The control and salinized plants were grown in two and four batches, respectively, containing 12 individuals each. This difference in population size between salinized and control plants was justified by the considerable increase in variability observed in Sorghum plants exposed to this NaCl treatment (Amzallag et al., 1995Go; Amzallag, 1998Go). A few individuals died following germination (two of the 24 controls and seven of the 48 salt-treated plants) and two other salt-treated plants died before flowering, which is why the population of control and salt-treated plants included 22 and 39 individuals, respectively. The results presented here are from the same experiment, in which all the plants from all the batches were grown simultaneously.

Measurements and calculations
The plants were harvested at the end of their lifecycle. Stem height (SH) was defined as the length between insertion of the first adventitious roots and the top of the spike, and ligule height (LH) as the height of the ligule of the corresponding leaf. The total seed weight (TSW) was measured and the average seed weight was determined after weighing three groups of ten seeds. The number of seeds (NS) was calculated as the ratio between total and average seed weight.

Relative increase in ligule height between two consecutive leaves has been calculated as follows:

(1)
where Lx and Ly are the ligule height of the two consecutive leaves x and y. Coefficient of variation (CV) of a parameter X was calculated as follows:

(2)
where STD(X) and AVG(X) is the standard deviation and the average of the parameter X calculated on the considered population.

The r coefficients are not parametric values, since their interval of variation increases proportionally to their distance from 1 and –1. For this reason, a difference between two r values close to 1 is not equivalent to the same difference between r values close to 0. However, according to Sokal and Rohlf (1981)Go, the r values may be converted in close-to-parametric values through a z transformation, according to the following formula:

(3)

For a parameter X, the connectance is calculated as the average of the absolute value of z for all the couples of variables between X and the other homologous parameters measured (Amzallag, 2000Go).

The value of the coefficient of correlation for linear regression (r) is influenced by the degree of freedom. Thus, it is impossible to compare the r coefficients (or their z transformation) between 22 control and 39 salt-treated plants without correcting the sample size effect. The r coefficients were assumed, at first approximation, to vary linearly within short confidence intervals. Thus, by using a detailed table of critical values of the correlation coefficient, it becomes possible to convert the r coefficients calculated on the population of non-treated plants (termed r20 because of the degree of freedom of the correlation) in r37 (the corresponding values for a population of 39 individuals, generating correlations with 37 df) by the use of the following formula:

(4)
where a20 and b20 are the lower and upper limit values of the interval of confidence in which may be inserted the r20 value. Similarly, a37 and b37 are the lower and upper values corresponding to the same confidence interval.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
NaCl-induced changes in reproductive characters
Exposure to 150 mM NaCl modified the end-cycle characters in Sorghum bicolor. Total seed weight, number of seeds, shoot DW, and weight of the four last leaves were strongly affected by the NaCl treatment while the total number of leaves and the average seed weight were slightly modified (Table 1). A comparison of the coefficient of variation (CV, see Materials and methods, equation 2) calculated on populations of control and salinized plants reveals that the range of variation is unchanged for some characters (plant height, shoot DW, number of leaves, and weight of the four latest blades), while it is enhanced by salinization in others (seed number, total seed weight, and average seed weight) (Table 1). An analysis of frequency of distribution for these characters reveals that the increase in CV is not caused by a symmetrical increase in variability around a single mean value (not shown). Rather, the phenomenon aims for diversification of the response in salt-treated plants, a phenomenon previously observed in Sorghum bicolor (Amzallag, 1998Go).


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  		Table 1. Mean and CV values of end cycle characters of Sorghum bicolor plants grown in the absence or presence of 150 mM NaCl

 
Changes in variability may be a consequence of modifications in the network regulating the expressed characters (Amzallag, 2001bGo). To test this point, the r coefficient for linear regression has been calculated for each possible pair of end cycle parameters considered in Table 1.

The significant correlations between all the parameters tested have been represented graphically. The number of significant correlations between characters is increased by the salinization treatment (Fig. 1). Moreover, qualitative changes in organization of the network occur in salt-treated plants. The number of leaves (a parameter proportional to duration of the vegetative phase of development) became isolated, while stem height now became linked to fertility (number of seeds) (Fig. 1).



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  		Fig. 1. Schematic representation of the significant correlations between parameters measured in populations of control and NaCl-treated plants. Data from Table 2. For more clarity, the total seed weight has not been represented in this graph. In both cases, it reproduces exactly the pattern of linkage of the seed number (except the link with average seed weight that disappears).

 

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  		Table 2. Relationships between all the possible couples of end cycle parameters

 
Only the significant correlations are represented in Fig. 1. However, changes in intensity of the linkage may also be considered. After standardization of all the r values (see Materials and methods, equation 4), changes in linkage between parameters are observed following salinization (Table 2). The level of linkage of each character with all the others has been quantified as connectance (see Materials and methods). Standardization of the r values before this calculation enables connectance of control and salt-treated plants to be compared. Following salinization, connectance is unchanged for shoot DW, and it is moderately reduced for the number of leaves, the average seed weight, and the final leaves weight. By contrast, NaCl strongly enhanced connectance of stem height, spike size, and seed number (Table 3).


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  		Table 3. Effect of NaCl on connectance of the end cycle parameters in Sorghum bicolor

 
For each character, the absolute value of the z coefficients (from which connectance is calculated) has been compared between salt-treated and control plants. A negative r value is observed for stem height and number of leaves (Table 3), confirming that the relationship between expression of these characters and others is strongly affected by salinity.

Discrete phases in Sorghum development
Change in the link between number of leaves and reproductive characters (Fig. 1) reflects a NaCl-induced modification of the linkage between vegetative and reproductive development. According to the phasic nature of grass development (see Introduction), an analysis of the relationship between vegetative and reproductive characters requires, first of all, the different phases to be distinguished.

Length of the blade has been measured for all the leaves of plants grown in the absence of NaCl. From kinetic analysis of this parameter, four ‘trends’ may be distinguished in the vegetative development of Sorghum bicolor (Fig. 2A). The blade length increases progressively towards a first maximum (trend I), and then it decreases (trend II), defining a first period in vegetative development. A second increase in blade length is later observed (trend III), and it is followed by a second decrease (trend IV) towards flowering, defining a second period in reproductive development. A similar phenomenon is also observed for salt-treated plants (Fig. 2B), although the first ascending trend is generally altered by developmental perturbations in leaves (termed DPL). This latter phenomenon has been related to maturation of the salt-adaptation response following this NaCl treatment (Amzallag et al., 1993Go).



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  		Fig. 2. Within-plant variations in blade length throughout vegetative development in Sorghum bicolor. (A) Control plants, (B) plants treated with 150 mM NaCl. Each curve symbolizes variations in blade length within a single plant. Four individuals are shown for each population.

 
The duration of each of the four trends strongly fluctuates among individuals exposed to the same conditions (Fig. 2). Thus, for each individual, each of the four trends has been characterized by the number of the last leaf of the trend (NLTI to NLTIV), as well as length of its blade (LBTI to LBTIV). The average NLT values, determined separately for non-treated and salinized plants, reveal that the duration of all the trends is not equally modified by salt-adaptation (Table 4). The trend most affected is the second one, followed by the third, while the duration of the first and fourth trends remains unchanged. The LBT values are also reduced in salt-adapted plants, but changes in length from one trend to another display the same range of magnitude in control and salt-treated plants (Table 4).


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  		Table 4. Characteristics of the four phases of vegetative development in Sorghum bicolor

 
In both control and salinized plants, a significant correlation is observed between LBTI and LBTII, and between LBTIII and LBTIV (Table 5). However, no significant correlation is observed between LBTII and LBTIII. This indicates that vegetative development should be separated into two distinct phases (see above). Nevertheless, the relationship between LBTII and LBTIV (Table 5) reveals that the first phase influences expression of the second one.


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  		Table 5. Relationship between LBT of the four phases

 
The ligule height (LH) of successive leaves increases progressively, both in control and salinized plants (Fig. 3A). However, this increment is not regular. A calculation of the relative increment in sheath length shows two distinct phenomena, while the 11th leaf represents the limit between them (Fig. 3B). Clearly visible in control plants (Fig. 3B, curve a), this dynamic is strongly perturbed by salinity (Fig. 3B, curve b), partly because of the perturbation in leaf unfolding during the first period. In many individuals, a negative value of increase in ligule height is observed, indicating that the ligule of the fifth leaf did not overcome that of the fourth one.



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  		Fig. 3. Average ligule height in Sorghum bicolor grown in the presence or absence of NaCl. (A) Average values; (B) relative increase in ligule height between two consecutive leaves. Curve a: control plants; curve b: plants exposed to150 mM NaCl. The relative increase has been calculated as described in the Materials and methods. Bars indicate the standard deviation calculated on the basis of the 22 or 39 individuals in control or salinized populations, respectively.

 
Shoot height and vegetative development
The link between expression of the reproductive characters and trends/phases identified during vegetative development has been investigated. In non-treated plants, a low linkage is observed between all the LH values and the LBT of each one of the four trends defined (Fig. 4A). However, a significant linkage (P <0.05 for z value higher than 0.327) appears between LH5 and the LBTIV, and between LBTII and LH of leaves 11–12. This reveals an influence of developmental factors during the second trend on late vegetative development.



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  		Fig. 4. z values of the relationship between blade length of the last leaf of each phase (LBT) and ligule height of the leaves. (A) Non-treated plants, (B) NaCl-treated plants. Continuous line and closed circles: relationship with LBT I; continuous line, open circles: relationship with LBT II; dashed line, closed squares: relationship with LBT III,; dashed line, open squares: relationship with LBT IV. All the z values are calculated after standardization of the r coefficients for linear regression as described in the Materials and methods. Correlations are significant (P >0.05) for z values higher than 0.327.

 
Salinization modified the dynamics of linkage between LBT and ligule height (LH). The four LBT values now correlate significantly with LH6, and an especially strong linkage is observed with LH9–LH12 (Fig. 4B). These findings confirm the existence of two distinct phases in vegetative development (Table 5). Moreover, they reveal a newly-emerging interference between LBTs and shoot elongation in salt-treated plants, especially marked during the third trend.

Linkage between vegetative and reproductive development
Regulation of shoot height is modified by salinity (Fig. 4). This observation may be related to the modified link between plant height and reproductive development observed in salt-treated plants (Tables 1–3GoGo; Fig. 1). To test this point, the link between vegetative development and reproductive characters has been investigated here.

In control plants, the level of linkage between LH and final stem height remains very low (Fig. 5, curve a). This indicates that the relationship between these two parameters is not trivial, even for LH of the last unfolding leaves. By contrast, two distinct linkages between LH and stem height are observed in salinized plants: the first one during early vegetative development, and the second one during unfolding of the last leaves (Fig. 5, curve b). This change suggests the emergence, in salt-treated plants, of a new linkage between stem height and size of the last-expanded leaves.



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  		Fig. 5. z value for the relationship between plant height and ligule height in Sorghum bicolor. Curve a: control plants; curve b: NaCl-treated plants. All the z values are calculated after standardization of the r coefficients for linear regression as described in the Materials and methods. Correlations are significant (P >0.05) for z values higher than 0.327.

 
In salinized plants, stem height not only correlates to vegetative characters, but is also linked to fertility (Fig. 1; Table 2), a character strongly perturbed by salinity (Table 1). This suggests that the perturbation in fertility may be related to the newly-emerging linkage between fertility and stem height in salt-treated plants. Hence, the relationship between fertility and LH has been measured for each leaf. A significant relationship is observed between LH5–LH6 and fertility (Fig. 6, curve a). It is similar to that observed between LH and final height (Fig. 5, curve b). However, no relationship is observed between LH of the last leaves and fertility (Fig. 6, curve a).



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  		Fig. 6. Involvement of plant height in the linkage between fertility and the ligule height of successive leaves in Sorghum bicolor exposed to 150 mM NaCl. Curve a: z value for the relationship between number of seeds and ligule height, curve b: z value for the relationship between plant height and ligule height, curve c: relationship between the residual value of fertility (calculated from its linkage with plant height) and ligule height. Correlations are significant (P >0.05) for z values higher than 0.327.

 
Comparing Figs 5 and 6 suggests that, during late vegetative development, control of fertility (initially determined during the first period of vegetative development) is now linked to stem height for its regulation. To test this, the residual value of fertility, determined from the correlation between stem height and number of seeds (NS), has been correlated to LH. Concerning the first leaves, the z value calculated for resSH(NS) evolves approximately in parallel to that calculated for fertility. This suggests that, until leaf 10, the link between fertility and stem height does not condition the linkage between fertility and LH. However, this situation is radically modified later, since the residual value of fertility does not correlate at all with LH after the ninth leaf (Fig. 6, curve c). This reveals that, after unfolding of the ninth leaf, control of fertility becomes conditioned by stem height rather than events inherent to vegetative development.

Fertility is reduced in salinized plants (Table 1). This change seems to be related to a modification of the relationship with characters such as stem height (Fig. 6). In order to confirm this, it was tested whether the link between fertility and vegetative development (reflected by the LBT values of the four trends) is also modified in a similar way by stem height. In salinized plants, LBT of the four trends generally correlate more significantly with fertility than with stem height (Table 6). The correlation even becomes significant for LBTIV. To test whether the linkage with stem height may perturb an initial relationship, the residual value of fertility (calculated from the relationship with stem height) has been correlated to the LBT values. A significant correlation is now appearing for the link with LBTI and LBTII, and the linkage with LBTIV is strengthened (Table 6). This suggests that, in salt-treated plants, the relationship between fertility and LBT values has been hidden by the newly-emerging relationship between stem height and fertility.


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  		Table 6. Comparison of the relationship with LBT of fertility, stem height or the residual value of fertility from correlation of this parameter with stem height in Sorghum bicolor exposed to 150 mM NaCl

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
Both in control and salt-treated plants, reproductive characters are conditioned by events occurring during a short period of early vegetative development, during the unfolding of the sixth to the seventh leaves (Figs 4–6GoGo). This period has already been identified as a critical period of high sensitivity to environmental factors (Caddel and Weibel, 1972Go; Amzallag et al., 1993Go; Amzallag, 1999Go), during which a reorganization of the regulation network may occur (Amzallag, 2001aGo).

According to fluctuations in blade elongation, two main phases should be distinguished in vegetative development, each one including an increment and a decrement in blade length of successive leaves (Fig. 2). This interpretation is strengthened by the lack of a relationship observed between LBTII and LBTIII, both in control and salinized plants (Table 5). It also agrees with previous observations (Vanderlip and Reeves, 1972Go) performed on the Sorghum genotype RS610 (the genotype studied here is the male parent of this F1 hybrid), that unfolding of leaves nine to ten corresponds to the initiation of stem elongation. This observation may explain the sudden drop in relationship between sheath and blade in leaves nine to ten (Fig. 4A).

If unfolding of the ninth to the tenth leaf corresponds both to stem elongation and to floral transition in the shoot meristem of Sorghum bicolor, a strong link between these two processes may be expected. Such a phenomenon is truly observed for NaCl-treated plants (Table 2; Fig. 6), but, surprisingly, no significant relationship is noticed between stem height and fertility in control plants (Table 2).

Under stress, a redundant network of interactions spontaneously evolves towards a hierarchical system (Amzallag, 2001bGo). This point is suggested here by the fact that, after unfolding of the tenth leaf, fertility becomes strongly linked to stem height in NaCl-treated plants (Table 2). Similarly, stem height, sheath length, and LBT values also became strongly linked in salt-treated, but not in control plants (Fig. 4). In this context, the effect of NaCl on variability (Fig. 2B; Table 4) may reflect a decrease in the level of redundancy in the network of regulation due to exposure to sublethal stressing conditions. Hence, it is possible that the linkage observed in NaCl-treated plants between stem elongation and fertility also exists in control plants, but its observation results from a decrease in redundancy in the regulation of fertility due to exposure to NaCl (as previously noticed by Amzallag and Seligmann, 1998Go).This interpretation is strengthened by the parallel ways of regulation of fertility existing in NaCl-treated plants, that are revealed by the relatively high values of r coefficients for the correlation between residual values of fertility (calculated from the relationship with stem height) and LBTs (Table 6).

This analysis reveals the multiplicity of effects of NaCl. Salinity induces perturbations in physiological processes directly involved in growth (such as cell division process, ion exchanges, osmoregulation, photoassimilation, and transport). Beyond this direct effect, NaCl also reduces growth through changes in the metabolism of plant growth regulators (PGRs), themselves affected by salinity. Moreover, beyond the disturbing effect on cellular physiology, NaCl may also induce modifications in the structure of the regulation network, especially during a critical period. This case is illustrated in the present study through the emergence of a new NaCl-induced relationship between the regulation of this parameter and that of stem height (Figs 1, 6; Table 6). It reveals that the direct toxic effect of NaCl on cell metabolism is not always the limiting factor for growth and development.

The between-organs network of interactions is conditioned by PGR production, transport, metabolism, and tissue sensitivity. For this reason, the changes in the regulation network observed here may be related to modifications in the PGR's physiology. The endogenous levels of PGRs in salt-treated plants and the meristem sensitivity to PGRs have not been measured here. For this reason, it remains impossible to determine the nature of the NaCl-induced modifications in PGR metabolism, transport, and/or mode of action. However, some indirect evidence points to changes in tissue sensitivity to gibberellins (GAs) and/or to modifications of their metabolism. A change in sensitivity to GA has previously been suggested following maturation of the salt-adaptation response in Sorghum (Amzallag, 2001aGo). In parallel, gibberellins are known for their influence on the characters analysed here; stem height, leaf elongation, and fertility in grasses (Jung, 1984Go; Tonkinson et al., 1995Go). In Sorghum bicolor, plant height, leaf elongation, and time of flowering are influenced by a few genes affecting GA metabolism (Pao and Morgan, 1986Go; Morgan et al., 1987Go; Beall et al., 1991Go; Lin et al., 1995Go; Foster et al., 1997Go). For these reasons, a change in GA metabolism and/or tissue sensitivity to GA following salinization is able to relate all the phenomena observed here, including modification of the link between stem height, length of the vegetative phase of development, sheath and blade leaf development, and fertility.

Through their influence on the whole-plant regulation network, NaCl-induced modifications may affect some developmental processes independently of the disturbing effect of NaCl on cell physiology. This confirms previous considerations about the lack of a direct relationship, in many cases, between the level of Na accumulation in tissues, cell sensitivity to NaCl, and tolerance at the whole plant level (Amzallag, 1997Go). Moreover, adaptation becomes a relative notion, inherent to each phase of development. A change occurring during a critical period may be adaptive for the emerging phenophase, but disturbing for the later developmental events. Consequently, measurement of adaptation through the number of viable seeds may be useful in ecology, but misleading in physiology.

Self-emergent properties are inherent to the formation of a network generating an autonomous dimension in development (Amzallag, 2000Go). This perspective challenges the classical assumption of stringent genetic control of development (Trewavas and Malho, 1997Go; Trewavas, 1999Go; Amzallag, 2001bGo; Katagiri, 2003Go). Moreover, the self-organized nature of the emerging network implies a high level of individuality that is hidden, in optimal conditions, by the redundancy existing between different pathways of regulation. This observation suggests that developmental adaptation and plasticity should be reconsidered in a new context, in which variability becomes a central factor for understanding the biological processes underlying the integrated plant response.


   Acknowledgements
 
All my thanks to the anonymous reviewers for their rigorous work on the manuscript and their pertinent advices and comments.


   Footnotes
 
Abbreviations: GA, gibberellic acid; LBT, length of the last blade of the trend; NLT, number of the last leaf of the trend; NS, number of seeds; SH, stem height; LH, ligule height.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Amzallag GN. 1996. Influence of parental NaCl treatment on salinity tolerance of offspring in Sorghum bicolor (L.) Moench. New Phytologist 128, 715–723.

Amzallag GN. 1997. Tolerance to salinity in plants: new concepts for old problems. In: Jaiwal PK, Singh RP, Gulati A, eds. Strategies for improving salt tolerance in higher plants. Oxford, New Delhi: IBH Publishing, 1–24.

Amzallag GN. 1998. Induced modifications in reproductive traits of salt-treated plants of Sorghum bicolor. Israel Journal of Plant Sciences 46, 1–8.

Amzallag GN. 1999. Individuation in Sorghum bicolor: a self-organized process involved in physiological adaptation to salinity. Plant, Cell and Environment 22, 1389–1399.[CrossRef]

Amzallag GN. 2000. Connectance in Sorghum development: beyond the genotype–phenotype duality. BioSystems 56, 1–11.[CrossRef][ISI][Medline]

Amzallag GN. 2001a. Developmental changes in effects of cytokinin and gibberellin on shoot K and Na accumulation in salt-treated Sorghum plants. Plant Biology 3, 319–325.[CrossRef]

Amzallag GN. 2001b. Data analysis in plant physiology: are we missing the reality? Plant, Cell and Environment 24, 881–890.[CrossRef]

Amzallag GN. 2002. The adaptive potential of plant development: evidence from the response to salinity. In: Läuchli A, Lüttge U, eds. Salinity: environment–plant–molecules. The Netherlands: Kluwer, 291–312.

Amzallag GN. 2004. Critical periods as fundamental events in life. Theory in Biosciences 123, 17–32.[CrossRef]

Amzallag GN, Seligmann H. 1998. Perturbation in leaves of salt-treated Sorghum: elements for interpretation of the normal development as an adaptive response. Plant, Cell and Environment 21, 785–793.[CrossRef]

Amzallag GN, Seligmann H, Lerner HR. 1993. A developmental window for salt-adaptation in Sorghum bicolor. Journal of Experimental Botany 44, 645–652.[Abstract/Free Full Text]

Amzallag GN, Seligmann H, Lerner HR. 1995. Induced variability during the process of adaptation in Sorghum bicolor. Journal of Experimental Botany 45, 645–652.

Beall FD, Morgan PW, Mander LN, Miller FR, Babb KH. 1991. Genetic regulation of development in Sorghum bicolor. V. The allele results in gibberellin enrichment. Plant Physiology 95, 116–125.[Abstract/Free Full Text]

Bourgeais-Chaillou P, Perez-Alfocea F, Guerrier G. 1992. Evolution ontogénique de la tolérance au NaCl chez le soja: comparaison des réponses au sel à deux stades de développement et chez les cals correspondants. Canadian Journal of Botany 70, 1346–1354.

Caddel JL, Weibel DE. 1972. Photoperiodism in Sorghum. Agronomy Journal 64, 473–476.

Dhingra HR, Varghese TM. 1993. Effect of salinity on flowering and male reproductive functions of chickpea (Cicer arietinum L.) genotypes. Biologia Plantarum 35, 447–452.

Dhingra HR, Varghese TM. 1997. Flowering and sexual reproduction under salt stress. In: Jaiwal PK, Singh RP, Gulati A, eds. Strategies for improving salt tolerance in higher plants. Oxford New Delhi: IBH Publishing, 221–245.

El-Saidi MT. 1997. Salinity and its effect on growth, yield and some physiological processes of crop plants. In: Jaiwal PK, Singh RP, Gulati A, eds. Strategies for improving salt tolerance in higher plants. Oxford New Delhi: IBH Publishing, 111–127.

Flowers TJ. 2004. Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.[Abstract/Free Full Text]

Foster KR, Lee IJ, Pharis RP, Morgan PW. 1997. Effects of ring D-modified gibberellins on gibberellin levels and development in selected Sorghum bicolor maturity genotypes. Journal of Plant Growth Regulation 16, 79–87.[CrossRef]

Katagiri F. 2003. Attacking complex problems with the power of system biology. Plant Physiology 132, 417–419.[Free Full Text]

Jung J. 1984. Plant bioregulators in cereal crops. Action and use. In: Ory RL, Rittig FR, eds. Bioregulators: chemistry and uses. ACS Symposium series, 257. Washington DC: American Chemical Society, 29–43.

Lin YR, Schertz KF, Paterson AH. 1995. Comparative analysis of QTLs affecting plant height and maturity across the Poaceae, with reference to an interspecific Sorghum population. Genetics 141, 391–411.[Abstract]

Morgan PW, Guy LW, Pao CI. 1987. Genetic regulation of development in Sorghum bicolor. Plant Physiology 83, 448–450.[Abstract/Free Full Text]

Munns R. 2002. Salinity, growth and phytohormones. In: Läuchli A, Lüttge U, eds. Salinity: environment–plant–molecules. The Netherlands: Kluwer, 271–290.

Pao CI, Morgan PW. 1986. Genetic regulation of development in Sorghum bicolor. Plant Physiology 82, 575–580.[Abstract/Free Full Text]

Romero JM, Maranon T. 1994. Long-term responses of Melilotus segetalis to salinity. I. Growth and partitioning. Plant, Cell and Environment 17, 143–148.[CrossRef]

Romero JM, Maranon T, Murillo JM. 1994. Long-term response of Melilotus segetalis to salinity. II. Nutrient absorption and utilisation. Plant, Cell and Environment 17, 1249–1255.[CrossRef]

Singh G, Jain S. 1982. Effect of some growth regulators on certain biochemical parameters during seed development in chickpea under salinity. Indian Journal of Plant Physiology 25, 167–179.

Slafer GA, Rawson HM. 1994. Sensitivity of wheat phasic development to major environmental factors: a re-examination of some assumptions made by physiologists and modellers. Australian Journal of Plant Physiology 21, 393–426.[ISI]

Sokal RR, Rohlf FJ. 1981. Biometry (2nd edition). San Francisco: Freeman and Company.

Solovev VA. 1960. About the individual salt tolerance and about formative processes in tomato. Fiziologia Rastenii 7, 222–227.

Strogonov BP. 1964. Physiological basis of salt tolerance. English translation from Russian by A Poljakoff-Mayber and AM Mayer. Israel Program for Scientific Translations, Jerusalem.

Tonkinson CL, Lyndon RF, Arnold GM, Lenton JR. 1995. Effect of the Rht3 dwarfing gene on dynamics of cell extension in wheat leaves and its modification by gibberellic acid and paclobutrazol. Journal of Experimental Botany 46, 1085–1092.[Abstract/Free Full Text]

Trewavas A. 1999. The importance of individuality. In: Lerner HR, ed. Plant response to stress: from phytohormones to genome reorganization. New York: Marcel Dekker, 27–42.

Trewavas A, Malho R. 1997. Signal perception and transduction: the origin of the phenotype. The Plant Cell 9, 1181–1195.[CrossRef][ISI][Medline]

Vanderlip RL, Reeves HE. 1972. Growth stages of Sorghum. Agronomy Journal 64, 13–16.[Abstract/Free Full Text]


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