A new beginning for biodiversity . . .

Earlier this week, I enjoyed—on catch-up TV—the third episode (about South America) of David Attenborough’s latest series on the BBC, Seven Worlds, One Planet. Here’s a taster of this wonderful series.

Once again, Sir David has treated us to a feast of images from the natural world, accompanied by his typical understated but informative commentary. And, as I was saying to Steph afterwards, cinematic technology such as drones with HD cameras has added a new dimension to natural history storytelling.

Most natural history programs routinely highlight loss of biodiversity (and its causes such as climate change), and Seven Worlds, One Planet is no exception. We live on a species-rich planet. But with so many programs about the natural world appearing on our screens, do we take for granted the diversity of nature and its millions of animal, plant, fungal, and microbial species?

Apart from Seven Worlds, One Plant, a couple of other biodiversity-related items on the radio have caught my attention in recent weeks.

The first, at the beginning of November, was an item on the early morning Today news and current affairs program on BBC Radio 4 (that I listen to in bed as I enjoy my early morning cup of tea) about an initiative to unravel the genetic code of all known 60,000 species of eukaryotes [1] in the United Kingdom.

Known as the Darwin Tree of Life Project (a most appropriate name!) it’s the UK arm of a worldwide initiative, the Earth BioGenome Project (EBP) to sequence the genomes of all 1.5 million known species of animals, plants, protozoa and fungi on Earth. That’s some challenge!

Each day, Charles Darwin would take a stroll along the Sandwalk at the bottom of his garden, where ideas about species and evolution not doubt swirled around his mind.

Why is the Darwin Tree of Life Project only possible now?

As stated on the EBP website: Powerful advances in genome sequencing technology, informatics, automation, and artificial intelligence, have propelled humankind to the threshold of a new beginning in understanding, utilizing, and conserving biodiversity. For the first time in history, it is possible to efficiently sequence the genomes of all known species, and to use genomics to help discover the remaining 80 to 90 percent of species that are currently hidden from science.

But also cost. Since the very first genome was sequenced in 1995 (of a pathogenic Gram-negative bacterium) the costs of sequencing have plummeted making it now economically feasible to even contemplate a project on the scale of the Darwin Tree of Life Project.

The UK component (launched on 1 November) is led by the Wellcome Sanger Institute in Cambridge in collaboration with Natural History Museum in London, Royal Botanic Gardens, Kew, Earlham Institute, Edinburgh Genomics, University of Edinburgh, EMBL-EBI (the European Bioinformatics Institute), and others. It is estimated that the project will take ten years to complete, costing £100 million over the first five years.

Dr Ken McNally

Molecular genetics and genomics have come a long, long way in just a few years. Just read the excellent 2014 analysis [2] by my former IRRI colleague, molecular geneticist Ken McNally how the latest developments in genomics (and related techniques) could contribute towards the conservation and use of biological diversity. And I’m sure things have progressed since Ken gazed into his ‘omics’ crystal ball just five years ago.

It’s remarkable how the science has accelerated in just a few decades. I completed my PhD under the supervision of Jack Hawkes, one of the world’s leading potato taxonomists and genetic resources conservation pioneer. In the 1960s (with colleagues from the immunology department at the University of Birmingham) he demonstrated that serology [3] could help clarify relationships between wild potato species (genus Solanum) [4].

As a graduate student at Birmingham in the early 1970s, I used a technique known as gel electrophoresis to separate potato tuber proteins, using the resultant patterns (position, and presence or absence) to better understand the relationships of different classes of cultivated potato.

Since the 1980s several different classes of molecular markers have been developed, and today—through whole genome sequencing—we can begin to decipher the complex relationship between genetic code and phenotypic and physiological diversity. We are beginning to explain better why species are different and how they are adapted to their environments.

My own research at IRRI and in collaboration with former colleagues Brian Ford-Lloyd, John Newbury, and Parminder Virk at the University of Birmingham in the mid-1990s, used molecular markers to analyse the diversity of rice varieties [5].

Another of the Birmingham-IRRI papers [6] was among the first (if not the first) to show a clear (and predictive) relationship between molecular markers (in this case RAPD markers) and appearance and performance of rice plants in the field.

Much of this rice research was aimed at understanding the diversity within a single species, Oryza sativa, which is grown over millions upon millions of hectares across the world. With hindsight, that research looks quite primitive, even though it was cutting edge at the time. Since the rice genome was first sequenced at the turn of the millennium, things have moved on apace, and more than 3000 genomes have been analysed to understand rice diversity.

But the Darwin Tree of Life Project will look across species, and hopefully keep a careful track of exactly which specimens/individuals are sequenced.

So, this brings me to the other radio broadcast I mentioned earlier. It was a discussion—about hybridisation between species—in the regular Thursday night In Our Time program, hosted by that doyen of broadcasting, Lord Melvyn Bragg with three biologists: Professor Steve Jones, Emeritus Professor of Human Genetics at University College London; Dr Sandra Knapp, from the Natural History Museum and a specialist in the taxonomy of the nightshade family, Solanaceae (that includes potatoes, tomatoes, eggplants, and many more); and zoologist Dr Nicola Nadeau of The University of Sheffield University. You can listen to that discussion here.

I found this discussion particularly interesting because in much of my research on potatoes, various legume species, and rice over many years I studied the relationships between species, and their ability to hybridise.

From the outset, Melvyn Bragg was working from the premise that species are distinct and rarely hybridise. That’s a reasonable point of view to take. After all, we can describe and identify millions of species based on the commonality of appearance (morphology) that individuals of one species share and make them different from other species. Like breeds with like.

Hybrids are less common between different animal species. Breeding behavior is a powerful isolating mechanism between species.

In plants, hybridisation is more common. However, there are many pre- and post-fertilization mechanisms that reduce the potential for hybridisation. It doesn’t matter if one can bring different species into cultivation alongside and successfully produce hybrids. In nature, many species never come into contact with each other because they grow in different habitats (in the same or different geographical regions). If they do grow in close (or relatively close) association, different species may not be reproductively compatible. Pollen from one species may fail to germinate on another or, if germinating, fail to achieve fertilization. Hybrid embryos may fail to develop, or even if hybrid seeds are formed, the plants are weak and fail to survive.

In the fluorescence images below (from pollinations between different tomato species that I used in class experiments with some of my students when I was teaching at Birmingham in the 1980s), a compatible pollination is shown in the images on the left and bottom. The other two images show poor pollen germination and growth in incompatible pollinations. Yet one or two pollen tubes have grown ‘normally’.

So, hybrids do occur, and are often successful in disturbed habitats that do not favor one parent or the other. There is a potential for species to expand their gene pools by exchange of some genetic material—or introgression, as it is called—that I described in one of my first blog posts in 2012.

Thank goodness plants can and do hybridise. As Steve Jones pointed out during the discussion, much of agriculture depends on ancient hybridisations and our ability to exploit cross compatibility between species. Wheat, one of the most important staple crops worldwide, is an ancient hybrid between three grass species. Potatoes evolved following crosses between different species (sometimes with different chromosome numbers) and hybrids were maintained by farmers since potatoes are grown vegetatively from tubers, not from seeds. Once a hybrid is formed then it can be maintained indefinitely through tubers.

Through hybridisation between cultivated varieties and wild species important characteristics or traits such as disease resistance can be added to the crops that farmers grow.

Just take this example from rice, showing the pedigree of the variety IR72 that was released in 1990. Many landrace varieties were crossed to produce this variety. But also very importantly, a wild rice, O. nivara (a close relative of O. sativa with which it crosses easily, and in the same genepool – see diagram below) was the source of resistance to grassy stunt virus, and it was this resistance that made IR72 such a successful variety.

One of the most important biodiversity initiatives in recent years has been the Crop Wild Relatives Project, started in 2011, managed by the Crop Trust with the Royal Botanic Gardens, Kew and many partners around the world. It is funded by the Government of Norway.

The project has a number of priorities including collection of crop wild relatives and their conservation around the world. But also evaluation and pre-breeding, exactly the same type of approach I used in my own studies on species relationships. This research aims to determine the gene pools (GP on the diagram below) of crops and their wild relatives (a concept developed by Jack Harlan and JMJ de Wet in 1971 [7]), and provides plant breeders with useful and important information about the value of different wild species, and what traits can be exploited for greater adaptation.

These are exciting times for the collection, conservation, evaluation, and use of the many species of crop wild relatives. With regular access to this valuable germplasm in genebanks around the world, and data on how they can be hybridised, and with the additional information about plant genomes, then plant breeders can begin to use these species more strategically, even using GM approaches. However, the cultivation of GM crops is banned in many countries including the countries of the European Union (one of the biggest mistakes the European Union has collectively made), even though these GM technologies can significantly reduce the time and effort required to transfer useful traits from one species into another.

Scientists have many tools in the plant breeding toolbox. It all starts with a seed, collected from nature, studied in the laboratory, and conserved in genebanks. There’s hope yet.

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[1] Eukaryotic species are defined as organisms whose cells have a nucleus enclosed within membranes, unlike prokaryotes, which are unicellular organisms that lack a membrane-bound nucleus, mitochondria or any other membrane-bound organelle (Bacteria and Archaea).

[2] McNally, KL. 2014. Exploring ‘omics’ of genetic resources to mitigate the effects of climate change. In: M Jackson, B Ford-Lloyd and M Parry (eds.) Plant Genetic Resources and Climate Change. CABI climate change series 4, CABI Wallingford.

[3] See Hawkes, JG (ed.) 1968. Chemotaxonomy and Serotaxonomy. Systematics Association and Academic Press, London. pp. 299.

[4] Hawkes published several immunological studies in the mid- to late 60s on North American and Mexican species of potato, with Richard Lester, one of his PhD students (and later Lecturer in the Department of Plant Biology at Birmingham).

[5] Virk, P.S., B.V. Ford-Lloyd, M.T. Jackson & H.J. Newbury, 1995. Use of RAPD for the study of diversity within plant germplasm collections. Heredity 74, 170-179. PDF

[6] Virk, P.S., B.V. Ford-Lloyd, M.T. Jackson, H.S. Pooni, T.P. Clemeno & H.J. Newbury, 1996. Predicting quantitative variation within rice using molecular markers. Heredity 76, 296-304. PDF

[7] Harlan, JR and JMJ de Wet, 1971. Toward a rational classification of cultivated plants. Taxon 20, 509-517.

The beauty (and wonder) of diversity

June 1815. British and allied troops muster in Brussels (then part of the United Netherlands) as the Duke of Wellington prepares to meet Napoleon at the Battle of Waterloo.

The troops are in good spirits, the social life of high society thrives, even as troops march to the front, with officers being called away to their regiments from the Duchess of Richmond’s Ball on the eve of the battle. The weather is fine, although it would deteriorate dramatically over the course of the battle in the next day or so.

Arriving in Belgium, one soldier commented on the productivity of  the local agriculture: I could not help remarking the cornfields today . . . they had (as I thought) a much finer appearance than I had seen in England, the rye in particular, it stood from six to seven feet high, and nearly all fields had high banks around them as if intended to let water in and out, or to keep water out altogether – but the rich appearance of the country cannot fail to attract attention.

Another cavalry officer wrote: I never saw such corn [probably referring to wheat] 9 or 10 feet high in some fields, and such quantities of it. I only wonder how half of it is ever consumed.

These are among the many contemporary commentaries in Nick Foulkes’ entertaining account of the social build-up to Waterloo. So what does all this have to do with the beauty (and wonder) of diversity?

Landrace varieties
Well, they are actual descriptions, almost 200 years old, of the cereal varieties being grown in the vicinity of Brussels.  Once upon a time, not too long ago before plant breeding started to stir up genetic pools, all our crops were like those described by soldiers off to fight Boney. We often refer to them as farmer, traditional or landrace varieties which have not been subjected to any formal plant breeding. You also hear the terms ‘heritage’ or ‘heirloom’ varieties, especially for vegetables and the like. Landrace varieties are highly valued in farming systems around the world – and the basis of food security for many farmers who grow them. However, in many others they have been replaced by highly-bred and higher yielding varieties that respond to inorganic fertilizers. The Green Revolution varieties released from the 1970s onwards, such as the dwarf wheat and rice varieties championed by pioneers such as Dr Norman Borlaug, bought time when the world faced starvation in some countries.

Now I’ve been in the business of studying the diversity of crops and their wild relatives almost all my professional life: describing it; assessing its genetic value and potential; and making sure that all this genetic treasure is available for future generations through conservation in genebanks.

The nature of diversity
But it wasn’t until the early 20th century – with the work of  Nikolai Vavilov and his Russian colleagues, and others that followed in their footsteps – that we really began to understand the nature and geographical distribution of diversity in crops. Today, we’ve gone the next step, by unraveling the secrets of diversity at the molecular level.

This diversity has its genetic basis of course, but there is an environmental component, as well as the important interaction of genes and environment. And I’m using a wide definition of ‘environment’ – not just the physical environment (which we think of in terms of growing conditions governed by geography, altitude, soil and climate) but also the pest and disease environment in which crops (and their wild relatives) evolved and were selected by farmers over centuries to better fit their farming systems. Landrace varieties that are still grown today in some parts of the world (or conserved in genetic resources collections) are extremely important sources of genes for adaptation to a changing climate for instance, or resistance to pests and diseases, as we have highlighted in our forthcoming book.

My own work on potatoes, rice and different grain legumes aimed to understand their patterns and origins of diversity, as well as the breeding systems which molded and released that diversity. I’ve been fortunate to have the great opportunity of working with or meeting many of the pioneers of the genetic resources movement, as I have described in other posts in this blog. But at the beginning of my career I became interested in studying crop diversity after reading the scientific papers of a group of botanists, Jens Clausen, David Keck and William Hiesey at Stanford University  (and others in Europe) who undertook research to understand patterns of variation in different plant species and its genetic and physiological underpinning.

These Californian pioneers studied several plant species found across California (including Achillea spp. and Potentilla spp.), from the coast to the high sierra, and planted seeds from each of the populations in different experiment stations or ‘experimental gardens’ as they came to be known. They described and determined the physiological and climatic responses in these species – and the genetic basis – of their adaptation to the different environments. The same species even had recognizable morphological variants typical of different habitats.

Experimental gardens established by Clausen Keck and Hiesey at three sites across California to study variation in plant species.

Interesting research has also been carried out in the UK on the tolerance of grasses to heavy metals on mine spoil heaps. Population differentiation occurs within very short distances even though there may be no morphological differences between tolerant and non-tolerant forms. Researchers from Aberystwyth have collected grasses all over Europe and have found locally-adapted forms in rye grass (Lolium) for example, which have been used to improve pasture grasses for British agriculture. But such differences in these and many other crops can often only be identified following cultivation in field trials where the variation patterns can be compared under the same growing conditions (following the principles and methods established by Clausen and his co-workers), and the data analysed using the appropriate statistical tests.

I began my work on genetic resources in 1970. I quickly realized that this was the area of plant science that was going to suit me. If I wasn’t already hooked before I moved to Peru, my work there at CIP on potato landrace varieties in the Andes (where the potato originated) convinced me I’d made the right decision. The obvious differences between crop varieties are most often seen in those parts of the plant which we eat – the tubers, seeds and the like, the parts which have probably undergone most selection by humans, for the biggest, the tastiest, the sweetest, the best yielder. Other traits that adapt a variety to its environment are more subject to natural selection.

Patterns of diversity are so different from one crop species to another. In potatoes it’s as though a peacock were showing off for its mate – you can hardly miss it, with the colorful range of tuber shapes but also including differences in the color of the tuber flesh. Modern varieties are positively boring in comparison. Who wouldn’t enjoy a plate of purple french fries, or a yellow potato in a typical Peruvian dish like papa a la huancaina. Such exuberant diversity is also seen in maize cobs, in beans, and the squashes beloved of Americans for their Halloween and Thanksgiving displays.

Many of the other cereals, such as wheat, barley, and rice are much more subdued in their diversity. It’s much more subtle – it doesn’t hit you between the eyes like potatoes – such as the arrangement of the individual grains, bearded or not, and color, of course. When I first started work with rice landraces in 1991, I was a little disappointed about the variation patterns of this important crop. Little did I know or realize. Comparing just a small sample of the 110,000 varieties in the IRRI genebank collection side-by-side it was much easier to appreciate the breadth of their diversity, in growing period, in height, in form and color, as I have shown in the video included in another post. Just check the field plantings of rice landrace varieties from minute 02:45 in the video. Now there are color differences between the various grains, which most people never see because they purchase their rice after it has been milled.

From a crop improvement point of view, this easily observable diversity is less important. It’s the diversity for yield, for resistance to pests and diseases, and the ability to grow under a wide range of conditions – drought, submergence, increased salinity – that plant breeders seek to use. And that’s why the worldwide efforts to collect and conserve this diversity – the genetic resources being both crop varieties and their related wild species – is so important. I was privileged to lead one of the major genetic resources programs at the International Rice Research Institute in the Philippines for 10 years. But the diversity programs of the other centers of the CGIAR collectively represent one of the world’s most important genetic resources initiatives. Now the Global Crop Diversity Trust (which has recently moved its headquarters from Rome to Bonn in Germany) is not only providing some global leadership and involving many countries that are depositing germplasm in the Svalbard Global Seed Vault, but also providing financial support to place germplasm conservation on a sustainable basis.

Crop diversity is wonderful to admire, but it’s so much more important to study and use it for the benefit of society. I spent almost 40 years doing this, and I don’t have any regrets at all that my career moved in this direction. Not only did I get to do something I really enjoyed, I met some incredible scientists all over the world.