This is the extended abstract of my paper for the Second Silicon in Agriculture Conference which was held in Tsuruoka in Japan (Aug. 2002)
Silicon and Abiotic Stress
M.J. Hodson1 and A.G. Sangster2
1School of Biological and Molecular Sciences, Oxford Brookes University, Gipsy Lane, Headington, Oxford, OX3 0BP, UK; 2Division of Natural Sciences, Glendon College, York University, Toronto, M4N 3M6, Canada
The very fact that we are meeting for the “Second Silicon in Agriculture Conference
” suggests that the importance of silicon in agricultural systems is becoming more recognised. However, this is not the case in plant physiology, where the element is still rarely considered [1
]. The problem of interesting plant physiologists in an element that is often regarded as “non-essential” is quite a major one, and this is certainly the case when we come to consider the abiotic stresses. Relatively few researchers in this area have even dabbled with silicon, and even fewer have made a concerted attempt to understand its potential roles in stress physiology.
What are the Abiotic Stresses?
Before we go any further we should attempt to define the words “abiotic” and “stress”. The first of these is relatively simple to define and “abiotic” can be taken to mean “the nonliving components of the environment” [3
]. So the remit of this paper will not include stresses caused by plant pathogens or herbivores. The word “stress” is decidedly more difficult to define, and has been the cause of some controversy, but seems to be associated with strain [4
]. In the context of this conference we could define a stress as anything that causes a decrease in plant growth or yield. Plant stress physiology is a vast area of research, and one that now even has it's own web site, www.plantstress.com
. That site covers almost all of the major stresses, but if we want a complete listing, then we are best to consult the classic book on the topic [4
Silicon- plus or minus?
In the natural or agricultural environment most plants will obtain enough silicon for their needs from the soil. In some cases, however, silicon fertilizers are added to the soil to improve crop performance, and we will hear more about these at this conference. Moving into the laboratory many plant scientists conduct experiments in hydroponic culture as it is easier to control what the plants obtain from solution culture than in soil. They often leave Si out of their formulations altogether, and the plants must then survive with what they can get from Si contamination of water and chemicals. Usually these plants seem to grow reasonably well, but there may be all sorts of hidden effects of growing plants with low levels of silicon, and Epstein [1
] has gone so far as to call such plants “experimental artefacts”. Even those scientists who do acknowledge silicon to be an important element in plant nutrition often have a problem in deciding what is their control. In the context of stress physiology, the most common experimental set-up will involve plants grown at a range of silicon concentrations including “zero” (true zero is almost impossible to attain, and the term “silica minimal” is often used). All these groups of plants then have the same stress applied, and the aim is to see whether added Si increases the growth of the plants under stress. Most scientists would tend to regard the “silica minimal” plants as their control, as they are “treating” plants with Si in the other groups. But would it be better to regard the Si plus plants as the control, and the Si minus plants as the “treatment”, as the former are closer to “natural”? Maybe.
We will now reflect on the effects of silicon on each of the stresses in turn. The aims of this paper will be two-fold: to assess what is known of the effects of silicon across the range of abiotic stresses; and then to concentrate on one particular stress, aluminium toxicity, where there has been much progress in recent years.
Table 1 shows our rough guide to the progress so far on the effects of Si on abiotic stresses. The table is intended to show how much work has been carried out on a particular stress, and how much is known about the mechanisms of any Si effects. It is apparent that there is much more known in some areas than others, and some stresses have hardly been considered. Even where considerable work has been carried out (e.g. on aluminium), we are still far from a complete understanding of the mechanisms.
Temperature stress- heat, chilling, freezing
Relatively little seems to been known about the effects of silicon on the various temperature stresses. Recently, Wang Lijun (pers. comm.) has found that creeping bent grass plants that were grown with Si had lower leaf temperatures than those grown without Si, and that this increased heat tolerance. We are not aware of any work showing effects of Si on relieving stress in chilling sensitive plants. However, it has been suggested that silica deposition in the walls of palm leaves may favour supercooling, and thus increase tolerance to freezing stress [5
Wind and other physical stresses
It has long been known that silica deposition in the shoots of higher plants can have considerable strengthening effects [6
]. A lodging resistant wheat cultivar has been shown to have a higher Si content in the culm epidermis than a sensitive one [7
]. Deposition of silica in rice increases the thickness of the culm wall and the size of the vascular bundle, preventing lodging during typhoons in Japan [8
]. Deprivation of Si may result in plants with physical abnormalities, such as a decrease in roughness [9
Light- too little, too much
One can imagine situations where Si could be beneficial to plants growing where there is either too little or too much light, but there is certainly a paucity of work in this area. Kaufman and his co-workers speculated that leaf phytoliths might act as “windows” or “light pipes” bringing light to the leaf mesophyll cells and increasing photosynthesis. However, when this hypothesis was tested the data did not support the idea [10
]. Silicon-fertilized rice often has more erect leaves, and this has often led to suggestions that these plants would have greater canopy photosynthesis. However, individual leaves of Si-fertilized rice do not show increased photosynthesis, despite better growth [11
]. White hairs are well known to have reflective properties in groups such as the cacti, and undoubtedly light reflection is a mechanism for keeping xerophytic plants cool. Siliceous hairs would also probably reflect light, but any reflection would probably be due to hair colour rather than to Si per se
As far as we know there are no papers suggesting that Si can have an effect on tolerance to radioactivity. However, it does seem that rare earth elements are often associated with Si [12
] and it may be that radioactive elements, many of which are trivalent or quadrivalent, may become co-deposited with Si in the plant in a similar way to Al (see below).
Water- drought and waterlogging (anaerobiosis)
Although the relationship between water uptake, transpiration rate and silica deposition in the plant is well established [13
], there seems to be a distinct lack of work on the effects of Si on water stress. Similarly, any role(s) for silicon in alleviating anaerobiosis due to waterlogging are obscure, despite the fact that rice routinely grows in such environments, is a heavy silicon accumulator, and even has substantial Si deposits in the root endodermis [14
There is considerable evidence that silicon is beneficial for crop plants [1,2
,11], and it is now routinely added as a fertilizer for several silicon accumulating crops. Growth and yield reductions have frequently been reported when it is supplied in sub-optimal amounts. Deficiency of silicon may also have quite complex effects on other nutrients. For example, in cucumber growth enhancement by silicon depended on an imbalance in phosphorus and zinc supply .
There has been a considerable amount of work on the effects of silicon on mineral toxicity. This can be broken up as follows:
a) Salinity. There is a reasonable body of literature that suggests that Si can have beneficial effects for plants growing under saline conditions. It seems that Si restricts sodium uptake to the shoot of sensitive plants [16
,17], and the mechanism is by partial blockage of the transpirational bypass flow .
. Our understanding of manganese toxicity in general, and specifically the ameliorative effects of Si on toxicity, owe much to the Germans, W.J. Horst and the late H. Marschner. In cowpea Si nutrition reduced leaf apoplastic manganese content suggesting that Si modified the cation exchange properties of cell walls [19
]. Electron paramagnetic resonance has shown that Si decreased leaf manganese content, and decreased the accumulation of oxidation products in the leaves [20
c) Other heavy metals. There have also been relatively infrequent reports that Si can ameliorate the toxicity of various heavy metals. Until recently, the mechanism(s) behind these effects have been obscure, but it now seems likely that some type of co-precipitation, often in the cell walls, is involved [21
In the last ten years it is true to say that there has been more progress on the effects of Si on aluminium (Al) toxicity than any other abiotic stress. Why this has been the case is difficult to ascertain, but it may partly be due to the parallel interest in Al/Si interactions shown by chemists and animal scientists, stimulated by the pioneering work of J.D. Birchall and his colleagues in the late 1980's . There is no doubt that Al toxicity in plants is a major problem, both for agriculture on naturally acidic soils and for forest areas affected by acidic rain. Many publications have now shown that under some conditions added Si can ameliorate Al toxicity in hydroponic culture. Two reviews have considered Al/Si interactions [24
,25], and we will not reiterate all of this material here, but rather will concentrate on recent developments in this topic.
One of the key problems in researching Al and Si in plants over the last ten years has been that the basic chemistry of how Al and Si interact in solution has been a fairly controversial topic. It is known that at neutral pH, Al and Si form hydroxyaluminosilicates (HAS), and that the formation of HAS reduces Al toxicity. What happens at acidic pH has been unclear, and this is the range of most interest to plant scientists. It now seems, however, that improvements in both speciation modelling and experimental procedures are throwing some light on this topic [26
,27]. The formation of HAS at pHs of 4.0 and below has been shown to be negligible, and formation gradually increases as pH increases to pH 5.0 and beyond. These findings have considerable importance for agriculture on acidic soils.
Plant Growth Effects
It is now apparent that amelioration of Al toxicity by Si in hydroponic culture is a rule, and not an exception. The few cases in the literature where amelioration has not been found are probably due to workers using a low background pH. The other exception may be Al accumulating plants like the Old World shrub, Melastoma malabathricum
], but this needs confirmation. Three recent examples showing amelioration, at least under some conditions, concern rice [29
], barley [30
] and Holcus lanatus
The mechanisms behind the amelioration effect are still somewhat obscure even in experiments conducted in hydroponic culture. It now seems that bulk solution effects due to the formation of HAS can account for almost all amelioration at pH 5.0 and above, and almost none below pH 4.0. Between these two values HAS formation will be increasingly important as pH is increased. However, there is growing evidence that in planta effects are also involved:
a) When experiments have been conducted near pH 4.0 or below, and amelioration has still been observed, then we can only conclude that that bulk solution phenomena are not involved. For example amelioration was observed at pH 4.2 in Holcus lanatus
, and the authors went to great lengths to show that no HAS formed in their hydroponic solutions [31
b) In very Al-sensitive plants amelioration can be observed at very low Al and Si concentrations, well below levels where solution chemistry effects are likely. For example in the wheat cultivar, Scout 66, the toxicity caused by only 1.5 micromolar Al could be partially overcome by 5.0 micromolar Si [32
c) There has recently been a lot of interest in organic acids in relation to Al toxicity. Two papers have concerned Al/Si interactions. In the first it was shown that even under conditions where Si ameliorated Al toxicity, the addition of Si did not reduce Al-induced malate efflux [32
]. In the second paper it was found that Si could actually stimulate greater organic acid exudation in some plants [33
d) The one attempt so far to investigate Al/Si interactions in cell suspension culture showed that in rice Si caused no amelioration in cell culture, but a significant amelioration in intact plants [34
]. This suggests that organized plant structures may be necessary for amelioration effects to occur.
e) Finally, the number of cases of codeposition of Al with Si in plant tissues is increasing- this merits a section of its own.
Codeposition of Al with Si
At the same time that plant physiologists have been discovering the conditions under which Si can ameliorate Al toxicity, electron microscopists, using x-ray microanalysis, have been finding more and more cases where Al and Si are codeposited in plant tissues. It has even been suggested that these Al/Si deposits may represent a new type of biomineral . There are two main locations where Al/Si deposits have been found: in the roots, particularly of grasses and cereals that have been grown in hydroponic culture; and in the needles of conifers. Recent examples include: (a) our own work [35
,39] on Al/Si deposits in the needles of the conifers (Table 2). Silicon and Al levels vary with the species, but codeposition is commonest in the epidermis and transfusion tissue. (b) Al/Si deposits in Lotus pedunculatus roots . (c) an investigation of Al in phytoliths in the above ground tissues of 20 species (Gramineae, Cyperaceae, Ericaceae and Coniferae) . Only the woody species produced phytoliths containing much Al.
Ten years ago there were very few such examples of Al/Si codeposition, and now they have become almost commonplace. The key questions now concern the chemistry of the deposits (are they aluminosilicates?), and their role. Intuitively, we feel that sequestering toxic Al in an Al/Si deposit should be beneficial for plant growth, but there is still no proof!
In the Field??
Although there has been some work using silicate slag to decrease Al toxicity [e.g. 42
], and the results have been positive, there is not a lot known in this area. One of the problems will undoubtedly be distinguishing Si effects from those of raised pH. According to the latest data, even liming a suitable mineral soil at pH 4.0 with standard calcitic or dolomitic limestone will radically affect the speciation of Al, Si and HAS, leading to decreased Al toxicity. Adding additional soluble Si to an acidic soil (above pH 4.0) would also be expected to decrease Al availability through bulk solution effects. Even below pH 4.0 it is possible that in planta
effects will decrease Al toxicity. Hopefully in the next few years we will be able to take Al/Si interactions into the field. If we can, then the benefits for agriculture on acid soils may be considerable.
We conclude that there is still a lot to do! In many topic areas almost nothing is known, and even in areas where most progress has been made (e.g. aluminium), we are still far from understanding the mechanisms of any effects. As resources are not great we need to prioritise research goals, and concentrate our attention on a few topics, preferably those that will stand the best chance of increasing agricultural production under stress conditions.
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