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Vol 20, No. 07, July 2016   |   Issue PDF view/purchase
Efficient Light-Harvesting of Plants: Conversation with Professor Alexander Ruban
APBN editor, Carmen met Professor Alexander Ruban, who was invited to give a presentation of the dynamic light harvesting membrane, at 4th International Workshop on Solar Energy for Sustainability: Photosynthesis and Bioenergetics held in Nanyang Technological University (NTU), Singapore last March.

Professor Alexander Ruban is a professor cum research fellow at Queen Mary, University of London. His lab focuses on the molecular mechanisms of light energy utilisation and management in the photosynthetic membrane. The major goal of his lab is to understand how biological matter is evolved to conduct a variety of intimate physical processes accompanying photosynthetic energy conversion and how structural properties of the photosynthetic light harvesting proteins govern flexibility and efficiency of photosynthesis.

Following the tribute session for Professor Jan Anderson FRS, Prof. Ruban talked about the mechanisms of light harvesting and photoprotection in photosystem II - the molecular mechanism of non-photochemical chlorophyll fluorescence quenching, NPQ, its regulatory factors and significance in protection of the reaction centre from the photodamage.

Amazed by the miracles of the natural dynamic molecular mechanism inside plants, we are glad to explore more on this topic through the interview with Prof. Ruban.

1. What led you to research on plant biophysics and molecular mechanism in plants? (Why did you chose to work on them?)

Plants are largely immobile organisms from outside, unlike animals, but they are very dynamic inside. Plant cells are entire biochemical laboratories for producing myriads of various useful substances that make them largely independent from other organisms. They also control the input of their only energy – light, that can be one moment very low and the next moment very high. I was fascinated by this, as Sir David Attenborough nicely put, ‘intimate life’ of plants.

2. Could you briefly explain what is non-photochemical quenching (NPQ) and PsbS as mentioned in your lecture?

Non-photochemical quenching (NPQ) is a process induced by light in plants. When plants (and some other photosynthetic organisms) are illuminated by high light, they cannot fully utilise the energy from Sun. That is the biggest problem in photosynthesis, the most important process that sustains life on Earth. In the case of higher plants, the photosynthetic reaction centres have limited capacity to release electrons into the electron transport chain, and receive electrons from the water splitting complexes. Water splitting complexes are oxygen evolving systems - they split water, evolve oxygen, and give electrons to the reaction centre, where an electron is then lost into the electron transport chain. Thus, the energy of electron is actually derived from energy of the sun.

However, if there is too much energy, reaction centres can be damaged by light. In order to reduce the amount of absorbed energy, plants have a specific mechanism which responds to certain factors. In the course of electron transfer, protons are transported across the thylakoid membrane to make energy for ∆pH required for ATP synthesis. This protonation of one site of the photosynthetic membrane affects the state of antennae of chlorophyll’s protein complexes which are not reaction centres but just like a funnel, they collect light and channel energy into the reaction centres. The higher number of protons, the more energy comes. The protein complexes evolved in shady environments, in oceanic waters, and in deep waters. Majority of them possess accessory pigments which are attached to separate proteins to transfer energy into the reaction centres. They get 200 times more frequent visiting of energy into the reaction centres - 200 times more electrons. If the light intensity is high and the plants have big antenna, the reaction centre complexes could get overwhelmed. In this condition, all unwanted photophysical reactions can happen.

Imagine you fill the bottle with water using a funnel. If you make holes in this funnel, it will leak, and you will see that less water will go into the bottle, and more would escape. Normal good antennae absorb light and keeps it for a certain duration, before transferring the light into reaction centres; but the one with leaking energy is like the funnel. NPQ causes antennae of plants to lose its efficiency; it doesn’t hold energy which is harvested for long, it absorbs energy and dissipates it into heat quickly. That is the principle of how NPQ works.

PsbS and xanthophylls exert control over NPQ by controlling the affinity of antenna complexes for protons. PsbS is a type of transmembrane protein, part of it is in the lumen, and part of it is in the other side of the membrane. This protein senses ∆pH. When protons are there, they protonate certain residues in PsbS and the PsbS responds by sending a message to shut the antennae. It’s a protein which controls the state of antennae as well of its NPQ state. If you don’t have this protein, nothing will happen. PsbS goes into the antennae and binds there. It is how it works in nature, but we don’t know why it binds and what it does yet.

Xanthophylls are carotenoids (plant pigments) which contain oxygen, and one type of them named violaxanthin. Under the presence of light, there are enzymes which can be activated by protons. With light, the particular enzyme is activated and two epoxy groups are removed from violaxanthin and it becomes zeaxanthin. This cycle makes the antennae more sensitive to facilitating the transition into the NPQ state.

The antennae becomes more plastic and more amicable to changing its state because of zeaxanthin, but the PsbS protein is the driver for this transition. We still don’t know how PsbS does it. This is a purely mechanistic question that is one of the questions my laboratory works on.

3. Do you mind sharing some of the other ongoing projects in your lab?

As what I mentioned earlier, one of the first discoveries is that PsbS interacts with antennae, a number of antenna protein types, not just one type. We study the details of such interactions and identify the preferred proteins of antenna with which PsbS interacts. This is one of the projects.

My other project is focused on diatom algae. Diatom algae are one of the major classes of microalgae of oceanic waters. They are extremely resilient to low light as well as high light intensity. They live in turbulent waters, and turbulent waters expose them to high light intensity or, in deep water - very low light. They do possess NPQ but they have completely different antennae and xanthophylls and have no PsbS protein. So it’s another model of how evolution puts forward a new solution, but the function is the same - protection. NPQ in them is much higher than in higher plants. One of the reasons is that most of their habitat is in dark waters and they live in dark environment. In experiments, we keep them in darkness for 50 minutes, and then expose them to 10 minutes of artificial light, subsequent 50 minutes darkness, and 10 minutes light, and so on, and they can survive in darkness, as long as you give them periodical light. They respond to this treatment and form large levels of NPQ. They ‘remember’ these periodic high light pulses and change everything in the membrane, in terms of antennae. Their antenna becomes more responsive to light and NPQ can reach up to 20. NPQ in higher plants is normally 2-4, but theirs is up to 20! Five times higher. The diatoms are simply the champions of NPQ!

Another project we work on is to determine how protective NPQ actually is; how much of NPQ is needed for the given light intensity. This is the closest biotechnological application we are dealing with. Agriculture is changing in our planet’s changing environment; new breeds of plants coming up and people want to grow plants in different areas and different countries. Imagine we go to a field, and ask “what is the light intensity here?” If we have data on light intensity, and data on how the light intensity will change, we can use this data in the lab experiments; using the new Valoya LightDNA system, we can reproduce the natural light environment and see whether this breed of plants can actually be happy to be planted in that place in the world. We could potentially recommend where to grow which cultures on. This can be applied for any photosynthetic crops, including algae.

4. Please tell us more about your collaboration with Microsoft & Valoya to produce this dynamic simulator, Valoya LightDNA. What is the current progress of this project?

The idea for the Valoya lights is to mimic the natural light environment in any part of our planet in terms of intensity, day length and spectral quality, and make it happen in laboratory or indoor conditions. Microsoft provides their software, and the databases, which contain data on light intensity, light quality and day length any day and time of the year. For example, if you input the coordinates of Singapore, just the simple numbers, and it downloads the meteorological data for Singapore, apart from the weather and clouds. The data includes the sun on a clear day, intensity, colour and dynamics. Morning sun has more blue light and evening has more red light. Then you can speed up the day to see how the colours change. I can program it from today’s date for a month, with light of Singapore, and use it with my test plants. Can you imagine how much money can be saved for agricultural companies to produce new breeds, and new varieties?

In addition, the artificial light in Valoya system is almost similar to natural light. Therefore, for example, if we grow beans which used to grow in fields near Santiago, they will grow exactly as they would in Santiago. Besides, we can experiment with colour to see if we can make them grow better. Let’s say the hypothesis is these beans need a little more far-red light colour because of some reasons such as this variety has much less Photosystem I in the photosynthetic membrane that absorbs this colour. If this is the case then we can potentially improve the plant performance with far-red light.

5. We talked about agricultural application, on top of that, how can we apply the knowledge from your lab to tackle the global climate change and global warming?

I think the most immediate usage of the knowledge is to forecast the state of crops in 10-20 years in various parts of the world. The global warming effects are different in various parts of the world. Some regions will stay okay for many years but some may suffer a lot. We can forecast how light and temperature changes affect plant growth in certain areas. We can give a prognosis and our recommendations to the companies, which are genetic engineering companies, or GM technology for plant species used for wood production, etc. With this protective NPQ technology, we can actually tell if this light intensity and fluctuations are good for plants and predict whether they will have detrimental effect if grow in those places with particular light properties. We can also model the cloud effect which modulates big fluctuations in light intensity. This can also affect plant growth and its response to light.

6. Could you briefly introduce your book The Photosynthetic Membrane and who is (or are) your target audience?

My book offers an insight into the molecular logic of nature using the example of the photosynthetic membrane. It explains at the molecular level the organisation of the complex photosynthetic machinery that performs a sequence of primary energy transformation events. This book focuses on the light harvesting phase of photosynthesis that is very efficient and yet flexible. The book also explains the essential features/definitions of life where one of the most important one is the energy requirement that is fulfilled almost solely by sunlight. It also shows the advantages and specific physico-chemical features of the nanoscale level of the organisation of the photosynthetic membrane. This book also contains a chapter considering the potential of the educational and practical applications of the knowledge obtained in studies of the photosynthetic membrane.

I addressed it to the final year undergraduate students of various biology specialisations as well as master and PhD students specialising in studies of photosynthesis. With this book, I also hoped to awake the interest of a broad audience of scientists and those who are attracted to the phenomenon of energy transformation in living nature.

Extract from the Govindjee’s review:

‘This book by Alexander Ruban is a fascinating story in a beautiful language on a topic that must be fully understood as we begin to manipulate the antenna size to increase productivity of plants, algae and cyanobacteria. … Ruban’s book is indeed a great book to read and re-read. I recommend that it be put on “Reading lists” for students in biology, biochemistry, biophysics as well as in biotechnology. It is indeed a refreshing book to read, and it has great quotes. What I enjoyed most was that it includes lots of basic dictums…. I strongly recommend “The Photosynthetic Membrane”, by Alexander Ruban, to all the advanced undergraduate and graduate students and even researchers of Plant Biology, Plant Sciences, Biochemistry, Biophysics, Molecular Biology, Biotechnology and Bioengineering. Further, all libraries around the World must acquire a copy of this book for their students and teaching faculty. It is indeed a beautiful and refreshing book at a time when we are just too busy with only technical aspects of a problem.’

7. What you wish to achieve from all your projects?

First of all I want to achieve a complete fundamental knowledge of how the light capturing processes evolved and work in the photosynthetic organisms and how the life matter evolved to ‘learn’ physics of light in general. I also want to see this knowledge applied in agricultural, ecological and renewable energy studies and applications. But first – the fundamental knowledge without which applications of half-baked results many times have been proved to be say the least useless.

About the Interviewee
Professor Alexander Ruban engaged in mechanistic photosynthesis research. He applies molecular spectroscopy, biophysics, biochemistry and molecular biology to important problems in plant physiology. Specifically, the role of the various components (proteins, lipids, pigments) and macrostructure in the functions and adaptive mechanisms of the photosynthetic membrane related to light harvesting and photoprotection in plants and algae. He is also interested in the universal properties of carotenoids in biological membranes, the molecular dynamics of these molecules in the modulation of membrane protein conformation and their functions (summarised in the recent book: Ruban, A.V. (2012) The Photosynthetic Membrane: Molecular Mechanisms and Biophysics of Light Harvesting. Wiley-Blackwell, Chichester, ISBN: 978-1-1199-6053-9).

His research has contributed to the fundamental understanding of the molecular design of the photosynthetic light harvesting machinery. His work contributed to hypothesis about the key role of LHCII antenna aggregation in the major photoprotective process in the photosynthetic membrane, NPQ and introduction of the concepts of light adaptation 'memory' via the allosteric action of the xanthophyll cycle, robust genetic design of the light harvesting antenna. His work led to discovery of the photoprotective molecular switch in the Photosystem II antenna which shortens the chlorophyll excited state lifetime protecting the photosynthetic membrane from photo-oxidative damage. He proposed that dynamics of antenna proteins is tuned by the polarity and structure of bound xanthophyll co-factors. Recently he established that the main photoprotective process in plants, NPQ, has an economic nature and developed a novel methodology for assessment of the photoprotective effectiveness of NPQ.

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