Aluminium-silicon interactions in higher plants: a brief personal history

How aluminium, silicon and two researchers are connected.

On 21st February 1989, I was working on the electron microscope in the Physiology Department of the Medical School in the University of Birmingham. By then I was on the last of my postdoctoral contracts, working with Denis Wilkins on aluminium (Al) toxicity and tolerance in conifers. At the time Al toxicity, caused by acidification of soils by acid rain in countries like Germany and Sweden, was thought to play a major role in the dieback observed in forests known in German as “Waldsterben.” I had made a bit of a speciality of x-ray microanalysis, and I was doing that in Birmingham, specifically looking at spruce roots from plants that had been treated with Al. I spotted something unexpected that day and made a note in my diary, “It seems that Al is frequently associated with Si (silicon) in the cell wall, and that it does get into one cytoplasmic compartment, the nucleus, where it is associated with phosphorus.” Later that year I visited the electron microscopy suite in Mount Sinai Hospital in Toronto where they had the most wonderful equipment for mapping elemental distributions, and sure enough, Al and Si were co-localised in the cortical cell walls (see Fig. 1). Why was I so excited? I had already been working on phytoliths (plant silica bodies) for ten years by 1989, but I had never seen Al associated with Si before. Could this be a mechanism for decreasing Al toxicity? I looked around the literature and found all sorts of leads in areas as diverse as fish biology and Alzheimer’s disease in humans, but there was not much on Al-Si interactions in plants. Little did I think at the time that this would form a major strand of my research, and that I would still be publishing on it in 2020!

Figure 1: Transverse section through the outer cortex and epidermis of a Norway spruce root. Scanning Transmission Electron Microscope (STEM) image, and x-ray distribution images for Aluminium (Al); Potassium (K); and Silicon (Si).

I moved from Birmingham to Oxford Polytechnic (now Oxford Brookes University) in September 1989. I soon persuaded my Canadian colleague, Allan Sangster, that Al-Si interactions in plants would be worth investigating. In the summer of 1991 we worked together in Toronto on this project. We conducted our first experiments on Al-Si interactions in sorghum and showed that Si really did ameliorate Al toxicity in that species. Moreover, we used x-ray microanalysis again and found Al and Si co-deposited in the root epidermal cell walls.

I first met David Evans on 8th October 1992, shortly after he arrived at Oxford Polytechnic as Royal Society Research Fellow. David was always more “cellular and molecular” while I was more “whole plant and environmental”, so we made (and make) a great combination. In 1992/3 I was supervising an undergraduate project student, Kim Hammond, who was looking at Al-Si interactions in barley, and getting good results. David suggested that we should apply for a Royal Society Summer Studentship for Kim to continue her work after she graduated. This was successful, and it enabled us to complete her work, showing again that Si could ameliorate Al toxicity. At the time David was an editor for the Journal of Experimental Botany, and his next idea was to review the whole topic of Al-Si interactions in plants in that journal before we conducted more work. The review proved quite popular, and by February 2020 had been cited 245 times according to Google Scholar.

So by 1995 we knew that under some circumstances Si could ameliorate Al toxicity in plants, but we had little idea of the mechanism. David and I were then fortunate to gain some grant funding, and were even more fortunate to have Kay Cocker (now Miller) as our Ph.D. student working on this topic. Kay cracked the problem for us with her highly innovative approach involving Al-induced malate exudation from wheat roots. To cut a very long story short it appeared that the amelioration mechanism involved the formation of non-toxic hydroxyaluminosilicates in the apoplast of the roots. We brought all this work together and wrote it up as a hypothesis. So far the hypothesis has had quite rigorous testing over more than 20 years and it has held up. David and I continued our work on Al-Si interactions for over ten more years, aided by our students Michelle Ryder and Subramaniam Prabagar. Meanwhile, Allan Sangster and I worked on mineral deposition in conifer needles, starting with white spruce, and then a number of other species (e.g. white pine; Fig. 2). Very frequently, we found Al-Si co-deposition in the epidermis or the transfusion tissue.

Figure 2. Mineral localization in a 2nd year needle of Eastern white pine (Pinus strobus), as determined by x-ray microanalysis. Micrographs illustrate the frozen planed face of a transverse section from 1 mm behind the tip. STEM image, and x-ray distribution images for calcium (Ca), silicon (Si) and aluminium (Al). Abbreviations: endodermis (en), epidermis (ep), hypodermis (hy) mesophyll (me), transfusion tissue (tr), vascular tissue (vt), xylem wall (xw).

As time went on David concentrated his efforts on the plant nuclear envelope, while I got involved in writing books (Fig. 3), in the use of phytoliths in archaeology and in palaeoecology, and then most recently in work on carbon sequestration. We both kept an eye on research involving Al-Si interactions, but neither of us were working on it. Then on 5th March 2019, completely out of the blue, I was contacted by Durgesh Tripathi, guest editor of a special edition of the Journal of Experimental Botany on plant silicon. Would I like to write a review article and on what topic? Straight away it flashed into my mind that I wanted to write an update review on Al-Si interactions in plants. I also knew who I wanted as my co-author; David Evans.

Figure 3. Left to right: Martin Hodson, David Evans and John Bryant. Taken in 2012 shortly after the publication of Functional Biology of Plants (Hodson and Bryant, 2012).

By 2019, David had risen to be Associate Dean of Research and Knowledge Exchange at Brookes, and was also heavily involved in his nuclear envelope work. When I approached him, I fully expected him to say he was too busy. But to my surprise he agreed to be co-author, provided we did the work in the summer vacation! In the 25 years since our first review, both Si and Al transporters had been discovered, and David’s knowledge of molecular biology was invaluable. We met together several times in the summer of 2019 and easily submitted the paper by the November deadline. Then we waited. Even experienced researchers worry about what might happen to their precious paper at the hands of referees and editors. But on the evening of 23rd December 2019, the email from the editor came with the decision, “minor corrections”. I quickly forwarded the email to David, saying here was an amazingly good early Christmas present for him. He agreed it was.

Our 1995 review came out in February that year, and exactly 25 years later in the same journal we are pleased to announce the publication of Hodson and Evans (2020). It has been quite a story so far. What will happen in the next 25 years?

Martin Hodson

Dr Martin J Hodson took his degree in Botany and doctorate in plant physiology from Swansea University. He then undertook postdoctoral research at Bangor University, The Hebrew University of Jerusalem, York University in Toronto and Birmingham University. In 1989, Martin settled at Oxford Brookes University where he rose to Principal Lecturer. He is now Visiting Researcher at Brookes, Associate Member of the Institute of Human Sciences at Oxford University and Operations Director for the John Ray Initiative. Martin's research focuses on plant silica and phytoliths. That has taken him into all sorts of interesting areas: archaeology, palaeoclimatology, biogeochemistry, cancer research, agriculture and food science.

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