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‘A greater awareness of the importance of Si in plants, especially on the part of experimental plant biologists, is bound to have beneficial synergistic effects beyond plant biology per se.’ (Epstein 1994).
Introduction
Studies concerning silicon (Si) in plants and soils have come of age. There was a time when papers on Si were rare events to be celebrated, but now it is impossible to keep up with the whole field. Emanuel Epstein, quoted above, had quite a lot to do with the explosion in research that has happened in the last quarter of a century. His major reviews (Epstein 1994, 1999) set the tone for much that has happened since. He was also correct that the work of plant biologists on Si has had beneficial effects well beyond plant biology. We have seen this impact in agriculture, archaeology, biogeochemistry, chemistry, food science, soil science, and palaeoecology, to name a few key areas. Quite quickly after Epstein’s reviews, a published monograph on Silicon in Agriculture appeared (Datnoff et al., 2001) and an updated collection was published 14 years later (Liang et al. 2015).
There have been very many reviews of aspects of plant and soil Si research in the last few years, and we will cite just a few here, and other, more specific, ones in the sections below. For a review concentrating on agricultural aspects of this topic, particularly in North America, see Tubana et al. (2016). Coskun et al. (2019) very much followed on from the reviews of Epstein, and considered some of the key controversies currently surrounding Si research. A detailed account of Si uptake, transport and deposition is provided by Mandlik et al. (2020). Greger et al. (2018) reviewed how Si influences soil availability and uptake of other nutrients by plants. Finally, the interactions of Si with essential and beneficial elements are covered by Pavlovic et al. (2021).
Our Special Issue is the first to focus on Si in Plant and Soil, but it is far from the first special edition we have seen in international scientific journals. In recent years we have noted these in Functional Ecology (Cooke et al. 2016), the Journal of Experimental Botany (Tripathi et al. 2020), and Frontiers in Plant Science (Cooke and DeGabriel 2016; Deshmukh et al. 2017; Hodson et al. 2020). Plants have had several small special editions, the largest of which was edited by Jörg Schaller and colleagues and included a major review of Si cycling in the soil (Schaller et al. 2021). In addition, the series of International Meetings on Phytolith Research (IMPR), which began in Madrid in 1996, have frequently produced proceedings, sometimes in books and not infrequently as special editions of journals. Zurro and Hodson (2018) documented all of these at the end of their paper under ‘Further Readings’.
As befits a Special Issue in Plant and Soil we wanted to bring together a collection that focussed on the interface between the plant and the soil, and so particularly looking at the rhizosphere. We are grateful to the authors who provided the papers for our Special Issue, and they well illustrate the variety of work that is now being carried out on Si in plants and soils.
Silicon uptake and deposition
One of the areas that has made most progress since the classic review articles by Epstein is Si uptake. The seminal paper by Ma et al. (2006) on a Si transporter in rice roots was the first of many articles on such transporters, and we now have a much better idea of how Si is moved across plant membranes. For a recent review of this topic see Mitani-Ueno and Ma (2021). Most of the Si taken up by plants is eventually deposited as solid amorphous silica bodies, often known as phytoliths. There have been fewer advances in our understanding of the deposition process than of Si uptake. It is now clear that there are two main types of phytolith, those where deposition is in the cell lumen, and those where silica is laid down on a carbohydrate matrix in the cell wall (Hodson 2016; Kumar et al. 2017). But many questions remain concerning the control of Si deposition.
In our Special Issue we included two papers that fit in the broad area of Si uptake and deposition. Most of the work carried out in this area has been conducted on plants grown in strictly regulated laboratory conditions, and there is far less available for field-grown plants. Schaller et al. (2022) investigated silicification patterns in developing wheat leaves and sheaths over a growing season in Germany. When they were just formed, leaves had relatively low Si concentrations, but this increased with time. Silica bodies and trichomes were particularly important sites of deposition. The work of Lu et al. (2021) was also conducted under field conditions, but this time in the tropical forest of Southern China. They investigated the effects of nitrogen addition on aboveground Si and phytolith concentrations in understory plants. Anthropogenic nitrogen deposition has enriched many areas of the world and has previously been shown to have modified the biogeochemical cycling of other elements. Lu et al. showed that nitrogen enrichment increased concentrations of silica and phytoliths in the leaves of understory plants, but had no effect on phytolith and plant available Si in the topsoil. We should point out that other workers (Johnson et al. 2021; Minden et al. 2021; Quigley et al. 2020) have found that increased soil nitrogen availability decreased shoot Si concentrations. Clearly more work is required in this area to explain the differences between these results.
Silicon isotopes
There are four Si isotopes in the natural environment: the three stable isotopes, 28Si, 29Si, 30Si, and the radioactive 32Si. The relative abundances of the stable isotopes are 92.23% (28Si), 4.67% (29Si), and 3.10% (30Si) on Earth. But isotopic fractionation events can occur which slightly change these abundances. Fractionation is defined as the relative partitioning of heavier and lighter isotopes between two coexisting phases in a system. Silicon isotopes have been much used by geochemists and those interested in using them as a proxy for environmental change, but there have been fewer investigations using these isotopes in higher plants (Leng et al. 2009). What is clear from studies with a variety of plants is that fractionation events occur as the isotopes are transported up the plant. The lighter isotopes are more reactive, and are incorporated into deposited silica lower down the plant, meaning that the heaver isotopes predominate towards the end of the transpiration stream. There is also a fractionation event as the isotopes are taken up into the root, and lighter isotopes seem to be preferred. Our Special Issue had one paper featuring Si isotopes, that by Zhou et al. (2022). The authors analysed Si isotopic fractionation in Si accumulators (rice, maize), intermediates (cucumber), and non-accumulators (tomato) grown in three different soils. All four species grown in any of the three soil types exhibited 28Si enrichment relative to the soil solution, confirming previous work that suggested that plant roots preferentially take up lighter Si isotopes. Within the shoot rice, maize and cucumber all showed the expected fractionation with heavier 30Si accumulating in the upper parts, but tomato showed no such fractionation, suggesting that non-accumulators may differ in their Si transport mechanisms.
Silicon and stress
Since the seminal review by Liang et al. (2007) it has become more and more evident that Si has major roles to play in the amelioration of abiotic stresses. This has made the area one of the most popular in plant Si research, and it is therefore not surprising that seven of the papers submitted to our Special Issue concern stress in some way. None of our papers concerned biotic stresses, and we might perhaps have expected this bias in papers submitted to Plant and Soil, as most publications concerning grazing or plant pathogens will be on shoots, and relatively few on roots and the soil environment.
The effects of Si on the responses of plants to drought is an important area, reviewed by Chen et al. (2018), and four papers in our Special Issue investigated this topic. Markovich et al. (2022) investigated the effects of drought in sorghum Lsi1 mutant plants which take up 1/15th of the Si that wild type plants do. They observed little difference in mutant and wild type plants under non-stressed conditions, but that under drought stress the mutant plants showed early stomatal closure which caused reduced transpiration. This then led to decreased growth under stressed conditions in the mutant. In a different approach, Wade et al. (2022) investigated the effects of watering regime on a barley landrace and cultivar. The amount of water the plants received was more important than frequency of watering in decreasing plant growth. Lowered water availability decreased Si uptake. It seems that sustained decreases in rainfall have a greater effect on Si uptake by plants, rather than episodic droughts followed by heavy rainfall events. This may be important as it indicates the kind of conditions under which Si supply is maintained, with consequent benefits for resistance to biotic and abiotic stresses. Teixeira et al. (2022) studied the effects of Si fertigation treatments on maize growing under two soil water regimes (adequate and severe drought). The three fertigation treatments were: sodium and potassium silicate stabilized with sorbitol; potassium silicate; and a control. Si fertigation increased Si uptake and growth of maize plants, even under drought conditions. Finally, Aktar and Ilyas (2022) investigated the effects of nanosilicab (a combination of a biofertiliser containing a number of bacterial strains and silicon dioxide nanoparticles), on wheat plants under control and drought conditions. Nanosilicab promoted the growth of wheat under all conditions, and was effective in relieving the effects of drought stress.
The amelioration of metal and metalloid toxicity by Si has been another major topic of research in recent years (Bhat et al. 2019). Our Special Issue included two papers within this general topic area, both featuring cadmium as a toxic element. An et al. (2022) investigated cadmium toxicity in maize plants and its amelioration by Si. They found that Si treatment reduced the toxic effect of cadmium on the plants, and also decreased the amount of the element transported into the shoot and the grain. The authors showed that Si treatment reduced daily intake of metal and health risk index for humans. Taking another approach, Linam et al. (2022), working on rice, investigated the effects of Si amendments (rice husks and husk biochar) on cadmium and arsenic uptake. These treatments significantly increased soil pore water and plant Si. However, the Si amendments had little effect on cadmium or arsenic concentrations in the plants, which seemed more related to water availability.
There has been much more work on the ameliorative effects of Si on metal toxicity than on its effects on elemental deficiencies. However, Benslima et al. (2021) observed that Si could mitigate the adverse effects of potassium deficiency in barley plants. The beneficial effects of Si were not seen through increased shoot potassium concentration and phenolic compound accumulation, but were mainly due to increased growth and photosynthetic activity.
Silicon in the rhizosphere
Whilst the papers in the other sections of this editorial were relatively easy to categorise, those in this section were less so, but all of the processes investigated here start in the rhizosphere and in the soil. There have been several recent review papers covering this area (de Tombeur et al. 2021b; Katz et al. 2021; Schaller et al. 2021). We will now assess the five papers published in our Special Issue.
Limmer et al. (2022) investigated the effects of Si additions to soil on iron plaque formation in the roots of rice. They found that the treatments had minimal effects on plaque quantities, although there were some differences in the timing of plaque formation. Rice is a heavy Si accumulator, and a very important crop, and it is not surprising that quite a number of investigations in this Special Issue concerned this species. The work of Ning et al. (2021) focusses on intercropping between rice and water spinach. Intercropping considerably increased absorption of Si by rice. The authors went on to investigate the mechanisms behind this phenomenon, and found that an interspecific rhizosphere interaction appeared to induce the upregulation of Si transporter genes in rice roots (OsLsi1, OsLsi2) and stems (OsLsi6), and also stimulated rice roots to secrete more organic acids thereby increasing available soil Si. Recently, de Tombeur et al. ( 2021a) highlighted the effect of root exudates, and specifically organic acids, on soil Si availability.
Two of the papers in this section concern interactions between roots and microorganisms. Putra et al. (2022) investigated the effects of Si treatment on Medicago truncatula inoculated with rhizobial strains of Ensifer meliloti. Nodule number per plant was increased with improved Si supply. The concentrations of nodule flavonoid concentrations, of foliar nitrogenous compounds and foliar carbon (C) were all increased in the Si treatments, but foliar Si was not. Johnson et al. (2022) studied the effects of Si treatment on arbuscular mycorrhizal fungal colonisation in the grass Brachypodium distachyon. They included both a wild type and a mutant, Bdlsi1-1, which takes up very little Si. The fungi did not affect Si uptake, but increased soil Si led to greater plant growth and phosphorus (P) uptake. The colonisation of the roots by arbuscular mycorrhizal fungi was suppressed in wild type but not in Bdlsi1-1 mutants.
The final paper in this section (Nakamura et al. 2022) was somewhat different as it did not concern plant responses to Si treatments, but focussed on the effects of siliceous trichomes on decomposition of leaf material in the soil. The authors investigated the decomposition of leaves of two species, Broussonetia papyrifera and Morus australis, in mesh bags that either permitted the entry of meso- and macrofauna or did not. B. papyrifera leaves had greater trichome densities than those of M. australis, and decomposed slower, but only in bags with a wide mesh size (5-mm) that allowed large decomposers to enter. It seems that siliceous trichomes reduced decomposition by the large decomposers and hints at effects of trichomes on C cycling in soil.
Silicon and carbon
Possibly the most controversial area of plant Si research at the moment is that concerning various aspects of the way Si interacts with C in plants and soils.
For many years, the dating of phytoliths using 14C had seemed a reasonably reliable technique, but the work of Santos et al. (2018) has thrown some doubt on it. They have suggested that “old carbon” originating from plant uptake from the soil is affecting dating results. However, others are less keen on this idea, and this has led to a vigorous debate (Piperno 2016; Zuo and Lu 2019).
Another area of controversy concerns C sequestration in phytoliths in soils, an idea that was first suggested by Parr and Sullivan (2005). Their calculations suggested that the amount of C sequestered in this way could be substantial on a global scale, and this could have importance in mitigating climate change. For some years this idea was largely uncontested, but then calculations of Reyerson et al. (2016) and others from this group, suggested that C sequestration in phytoliths is insignificant globally. The main problems have been the difficulties in determining the “true” concentration of C in phytoliths, and how quickly phytoliths dissolve over time. A major debate ensued which was documented by Hodson (2019), who suggested a number of topics that need to be addressed to help resolve the dispute. However, there are still papers being published which tend to ignore the issues that have been raised, and make bold statements about the efficacy of C sequestration in phytoliths (e.g. Song et al. 2022). It is worth noting that the recent 6th Assessment Report of the IPCC, Working Group 3, on mitigation of climate change considered C sequestration in soils in some depth, but did not mention phytoliths once (IPCC 2022). Some in the phytolith/ plant Si community may be certain of the importance of C sequestration in phytoliths, but the wider scientific world has yet to be convinced.
The final area in this section that we will cover is trade-offs between Si and C, and so-called substitution of one element for the other. The idea was first suggested by Raven (1983) as he calculated that using Si for structural support should be energetically favourable over using C compounds. However, it has only been in the last 12 years, since Schoelynck et al. (2010) promoted the idea, that this area has taken off to become a popular area of plant Si research. Even just within this Special Issue these trade-offs are mentioned by Johnson et al. (2022), Putra et al. (2022), Schaller et al. (2022), and Wade et al. (2022) in the context of their quite varied research topics. However, one paper, Hodson and Guppy (2022) had a specific focus on this subject, and pointed out some potential problems that need to be considered. In particular, the authors were concerned that we needed to relate Si and C trade-offs, often observed from whole organ analyses, to Si and C distributions at the cellular level. Moreover, they were worried about some of the language being used to describe this phenomenon, and with the use of the word “strategy” in a manner bordering on teleology.
Silicon fertilisers
As scientists have realised how significant Si is in plant nutrition the deployment of Si fertilisers has been increasing in many parts of the world and for a wide range of crops. Two reviews that have given significant coverage of Si fertilisers are those by Artyszak (2018) and Puppe and Sommer (2018). One of the key issues in Si fertiliser research in the context of plant nutrition concerns the availability and release of Si from the many, and increasingly various, products available on the market. An approved test was released to measure Si availability from solid products in 2013 (Sebastian et al. 2013) using a 5-day alkaline-salt extraction, but within two years questions were raised around how closely that test reflected plant recovery of Si from the applied products (Zellner et al. 2015). Many of the papers in our Special Issue applied some type of Si treatment, including three that we have already mentioned where the emphasis was more on the plant responses: one study concerning the effects of nanosilicab on drought stress in wheat (Akhtar and Ilyas 2022); work on Si fertigation in maize (Teixeira et al. 2022); and Linam et al. (2022) who studied rice husk and charred husk amendments and their impacts on cadmium and arsenic uptake in rice. Difference in Si availability from various products was demonstrated by Linam et al. (2022) where the highest Si concentration product was less soluble than untreated husks. There were, however, two papers where the focus was more specifically on the fertilisers themselves. Both of these papers concerned interactions with P availability. Gunnarsen et al. (2022) investigated the effects of glacial rock flour (GRF) amendments on P availability in an acidic tropical soil. The authors found that GRF did not improve P availability in the soil, but the Si released from the fertiliser did improve stress tolerance and wheat plant yield.
Finally, Rezakhani et al. (2022), working on wheat, examined the effect of Si fertiliser alone or in combination with phosphate-solubilising bacteria (PSB) on plant uptake of P and Si when grown in a calcareous soil with low available P. When treatments included both Si and PSB strains, increased shoot uptake of Si and P and wheat biomass was observed as compared to the control and treatments where either Si or PSB were applied alone. It is heartening to see innovation in product design that recognises that both microbes and plants play a role in releasing Si from soil and fertiliser products, and we hope that future rhizosphere research increases our understanding of ways to improve the startlingly poor solubility of many of the Si sources available on the market currently.
Conclusions and future prospects
We were very pleased to gather such a diverse and internationally representative set of papers for this Special Issue. Our authors listed their addresses as in Australia, Brazil, China, Denmark, Germany, Iran, Israel, Japan, Pakistan, Spain, Switzerland, Tunisia, United Kingdom, United States of America, and Uruguay. So, it appears that research on Si in plants and soils is now happening on every continent, with the possible exception of Antarctica. The assembled papers also represent the very wide range of topics that are now being worked on, far wider than we had even envisaged at the time of Epstein’s first review in 1994. Perhaps not too surprisingly, given the importance of Si for grasses and cereals, 13 of the 18 papers focussed on these species, including four on wheat and three on rice. Three papers featured dicot species, one looked at both cereals and dicots, and one had no species focus. Katz (2014) called for more Si studies on plants other than grasses, but obviously the bias is still there.
Clearly more progress has been made in some areas than others. So, we have a much better knowledge of Si transport in plants than we did 25 years ago, but studies of Si deposition have lagged some way behind. It is now well recognised that Si has major roles to play in the alleviation of stress in plants. We are only just beginning to understand some of the processes Si is involved in at the plant-soil interface in the rhizosphere. The whole topic of the way Si and C interrelate in plants has grown both in importance and in controversy in recent years. Fertilisers containing Si are increasing in significance, and a number of our papers reflected this, and studies on rhizosphere mobilisation of Si in soil and fertilisers will hopefully increase accordingly.
Looking forward, the future for research on Si in plants and soils looks bright. The growing recognition of the importance of Si in agriculture, and the links with many other fields, particularly archaeology and palaeoecology, will ensure that this is the case. The interdisciplinary nature of much of the work on Si makes it a very exciting area, even if it is almost impossible to keep up with everything that is happening!
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Acknowledgements
We are grateful to all the contributors to this Special Issue, and to the many anonymous reviewers who gave critical comments to improve the quality of the papers submitted. We are thankful to the Editor-in-Chief, Hans Lambers, for the opportunity to edit this Special Issue. Finally, we thank the Managing Editor, Lieve Bultynck, and all the staff from Plant and Soil for all their hard work that made the Issue a reality.
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MJH wrote the first draft of the editorial. CNG commented on the draft. Both authors agreed with the final draft.
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Hodson, M.J., Guppy, C.N. Editorial: Special issue on silicon at the root-soil interface. Plant Soil 477, 1–8 (2022). https://doi.org/10.1007/s11104-022-05514-1
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DOI: https://doi.org/10.1007/s11104-022-05514-1