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Down the Rabbit Hole: Genomics of tree health and adaptation – Richard Buggs, Evolutionary Biologist

Richard Buggs is a Professor of Evolutionary Genomics at Queen Mary, University of London (QMUL) and a Senior Research Leader at Royal Botanic Gardens Kew. His research uses evolutionary genomics methods to understand the basis of pest and pathogen susceptibility of plants. His main project explores the genomics of ash tree species and their susceptibility to the fungal disease, ash dieback (Hymenoscyphus fraxineus).

Please note the transcript has been edited for brevity and clarity.

FLG: Hello, everyone and hello, Richard. Welcome to the latest interview in the Down the Rabbit Hole series. Today, we’re going to be talking about trees, yes, trees, and how genomics is being applied in this often underappreciated area of research. So, Richard, if you could just start off by introducing yourself and telling everyone a little bit about what you do as well.

Richard: Thanks, Shannon. My name is Richard Buggs. I’m a Senior Research Leader at Royal Botanic Garden, Kew. I’m also Professor of Evolutionary Genomics at Queen Mary University of London. And as Shannon says, my research is mainly focused on the genomics of trees.

FLG: One of your main areas of research is looking at how genomics can be applied to understand the basis of pest and pathogen susceptibility in plants. Why is this area of research so important?

Richard: Well, it’s really a growth area, because unfortunately, globalisation is spreading pests and pathogens around the world very fast, not just of humans, but also of plants and animals. We’re really focused on the diseases that are coming and hitting our native tree species in the UK. Unfortunately, there’s more and more of these pests and pathogens coming in. We’re moving them around the world through global trade. Then, climate change also is exacerbating the problem. So, this is, unfortunately, a real growth area where more and more research is needed. I guess in the past, we’ve tended to think that trees just take care of themselves. But unfortunately, increasingly, we’re seeing that isn’t actually happening. We lost elm trees, back in the 1960s, as large trees in the landscape. And more and more other tree diseases have been coming in over the last few years.

FLG: One of your biggest projects is looking at the genomics of ash tree species. Why are trees, in general, so difficult to research in terms of their genetics?

Richard: Well, classically, when looking at plant genetics, people would be working on plants with an annual lifecycle, or even a life cycle with just a few weeks, like the model plant, Arabidopsis. And so, in those situations, it’s very easy to cross plants and then raise up a family from them and do a genetic map, and maybe do another family of another generation. You can also make recombinant inbred lines. So, you can have a line that’s got very little heterozygosity in it. And you can just study particular loci that you’re interested in. And of course, we can’t do that with trees, because they live so long, they don’t start reproducing until they’re several years old and they’re massive (we can’t just grow them in a growth chamber). So, in many ways, working with trees is actually much more like working with humans than like working with wheat or barley or the model plant, Arabidopsis. And so, we have to start thinking, well, are there methods that have proved useful in human genetics that we can use on trees? Because like trees, you can’t set up controlled crosses of humans that you decide you want to cross, you can’t raise up a generation in a year. All of the problems that we have with trees, we also have with humans. But of course, there’s been massive amounts of funding for research on human genetics. And so, we can benefit from that and pick up on many of the methods being used on humans and apply them to trees.

FLG: How have some of the advanced technologies helped with these challenges and allowed us to gain more insights into this area?

Richard: Well, it’s made issues in the past that we could not have tackled in a short space of three or four years into issues that we can now tackle in that time span. So, for example, my group wanted to find the genetic basis of resistance to ash dieback in our ash trees in the UK. We knew that some trees seemed to be surviving the fungus and studies in Denmark suggested that some of this had a heritable basis. In other words, there is a genetic basis for resistance to ash dieback. And so, we wanted to know what genes are actually involved. Because if we know what genes are involved, then potentially we could accelerate breeding programmes by having a genotyping platform to select trees with the alleles that we want to breed into populations. If there are lots of different alleles that are all contributing a little bit to resistance and if we can bring all of them together in a single lineage, then that hopefully will be a more resistant tree. So, in order to find those genetic loci, we of course, couldn’t set up crosses between different ash trees and then wait for the progeny to grow up and then test them for ash dieback resistance. That would take literally decades to do. But using approaches like genome wide association studies that have been developed very much with humans in mind, and also techniques of genomic prediction, which have been developed for livestock like pigs and cattle. Using these approaches, we can actually make much more rapid progress in discovering the genetic basis of resistance than we could have done with a linkage mapping approach. So, they’ve really helped us in that way.

FLG: What is the current landscape of ash dieback? Why did you specifically focus on ash trees?

Richard: Well, ash dieback is getting worse and worse at the moment in the UK. All over the country now, we can see trees dying back and dying off completely. This fungal disease was first discovered in the UK in 2012, although it was probably here before that. It spread across the whole of Europe, spreading from Poland westwards for the last 20 or so years. It’s really devastated ash populations throughout Europe, and in the UK. So, we actually started working on the ash genome in 2012, the Natural Environment Research Council gave me a grant then to do the first genome sequence of a British ash tree. Since then, we’ve built on that with bigger studies looking for resistance alleles as I mentioned. If there’s been any doubt in my mind whether or not this is a worthwhile problem to look at, this year has really confirmed it, because the ash dieback damage I’ve been seeing around the country this year is actually so much worse than it’s been in the past. Woodland owners and the Highways Agency and Network Railway are having to spend huge amounts of money removing diseased ash trees so that they don’t fall over on top of cars or on train tracks or on people. They are a major health and safety issue now because the pandemic has got to such a stage where lots of trees are dying off.

FLG: Why is it so important to ensure that we do control this?

Richard: Well, if we don’t do something, we potentially face a situation where we no longer have ash trees as a tree for planting in woodland forestry. Indeed, we are already at the stage where people don’t really want to plant ash. At the worst extreme, we could end up with no ash trees in the landscape a bit like what has happened with Elm. There are now very, very few elm trees in the British treescape because of Dutch Elm disease. Some of our research has been on this issue – how bad could it be? Could we lose all of our ash trees? The results are encouraging in that we don’t think we will lose all of them, there seems to be enough resistance out there. If our genomics work is correct, then it suggests that natural selection will be able to kick in, perhaps is already kicking in. And in the younger ash trees that are coming along, we are seeing a higher frequency (we hope) of alleles associated with ash dieback resistance. In some ways, the genomics work has given us a bit more optimism about ash than we had for elm trees, although things still look pretty dire. This isn’t really a case of being able to control ash dieback, that’s completely uncontrollable at this stage. It’s thinking about the future, and how we can ensure that we do have ash trees in the landscape in 50 or 100 years time. So, we’re definitely going to see a big, big dip in the ash population. But we’re hoping it will recover partly through natural selection, and also perhaps partly through a breeding programme. If we decide as a nation to do a breeding programme for ash, then we could use the genetic markers to rapidly breed ash trees with greater resistance to ash dieback and perhaps do that much more quickly than natural selection will be able to.

FLG: What are the driving forces of the spread of ash dieback? Are humans contributing to this spread?

Richard: Well, we definitely exacerbated its spread in the early years by the way we sourced saplings for planting. So, a lot of our ash trees for planting were sourced from the European continent. So, they were sold as British ash trees, because they had come from seeds from Britain. But those seeds were exported to the continent, and then they were grown up on the continent, and then brought back into the country. Many of them were coming back in with ash dieback already in them. So, there were definitely things we did to increase the rate of spread of ash dieback. On the other hand, it is a disease that is spread by spores that are windblown. It was inevitable once the European continent was infected, that it would come here and would blow across the channel. And so, all we did was accelerate the inevitable. It would have been very, very hard to have actually stopped the pandemic from reaching Britain, unfortunately,

FLG:  You work alongside Novogene. I know you mentioned that you’ve been using GWAS data. What other genomics tools are you using to investigate this? How are you being able to track this resistance?

Richard: Yeah, so we’ve been doing a lot of whole genome sequencing of different individuals with different levels of resistance to ash dieback. One method that we use to save money was a pooled approach. So rather than sequencing every individual separately, we put our ash trees into pools that came from the same seed source and had the same level of resistance to ash dieback. And so, for every seed source, we’d have about 40 more resistant trees and about 40 more susceptible trees. Then, we would sequence them all together to quite high coverage, but to much lower coverage than what we would have had to have used if we had done them each individually. Of course, we didn’t have to pay for the library prep for each individual either, we just had to do one library prep per pool. That enabled us to estimate allele frequencies in the different pools. We could do a genome wide association study based on those allele frequencies in the pools. So that saved us a lot of money, but got us quickly to candidate genes, which is what we were wanting. Then, we were able to use those candidates to do genomic prediction on trees that we had sequenced individually. That’s the main approach that we used initially. More recently, we’ve been studying a natural woodland in Surrey, in the UK. We have been doing individual genome sequences for each of those trees and predicting how susceptible they are genomically to ash dieback. And so, in that next stage of the work, we have been doing individual whole genome sequences. It really depends on how much money we can get at any particular time, of course, and on the drop in the cost of sequencing as well.

FLG: What have been some of the key findings? How will these findings help protect ash trees?

Richard: We’re very much hoping that these results will be able to inform a breeding programme. If we’re able to grow up lots of ash trees and then at a seedling stage, sample their DNA and genotype them and then predict which ones of them are worth growing on, then we could save time and space in a breeding programme which for trees does take up a lot of time and space. What we’d really like to do is develop lines of ash that flower very early. Then we can do something called rapid cycle breeding. This is something that’s been done in fruit trees. So, apple trees have been engineered so that they flower at a very young age. Then, using marker assisted breeding, you can take them through lots of generations of a breeding programme. And then in the final generation, you segregate out the transgenes that are causing early flowering. And you end up with a tree that’s not genetically modified but has been through an accelerated breeding programme that has used its natural genetic variation. If we could do that on ash that would really accelerate breeding programmes and enable us to develop increased resistance to ash dieback much faster using natural variation than we would be able to otherwise.

FLG: What are some of the key challenges that exist?

Richard: Well, the major challenge is the longevity and the size of the trees. One issue that’s a real challenge to all genomic prediction methods is how specific they can be to particular genetic backgrounds. So just because we found a set of alleles that are predictive of ash dieback resistance within the UK using the samples of trees we have, transferring those markers to other situations isn’t always straightforward. If we could find alleles that are always predictive of ash dieback resistance in any genetic background, then our results would roll out really well across the whole of Europe. But unfortunately, at this stage, we are struggling with this problem of the extent to which genomic predictions are genetic background context specific. So that’s like with any use of genomic prediction in breeding of livestock and crops. This is a big issue that we face.

FLG: You also work on birch and oak trees as well. What are you exploring in this area? How different are they in terms of the challenges working with these different species?

Richard: Well, with oak trees, our main emphasis is on trying to understand a complex syndrome of oak trees called acute oak decline. It’s a syndrome where the trees start to bleed in their trunks, they have this black goo coming out of cracks in their bark. Some trees recover, but some trees die of it quite rapidly. It’s particularly common in parklands around big country houses, which of course, are quite common in Britain. That’s a major concern for oak, which is our most important broadleaf species. Because it’s oak we’ve been able to get enough money to do lots of whole genome sequencing of individuals, we haven’t had to take a pooled approach. At the moment, we’re just gradually building up a really big set of whole genome sequences so that we can do a genome wide association study. At this stage, we don’t even know if there’s a heritable basis to resistance to acute oak decline. But conventional methods of working out if there’s heritability would be really difficult to implement. So, we’re actually trying to do a genome wide association study to work out if there’s heritability of resistance or not. Normally, you would have answered that question first. But because it’s oak trees, we can’t do that. And so, we’re having to take this genomic approach just to work out whether or not there is heritability of resistance.

FLG: What about your work on birch trees?

Richard: In birch trees, we’ve had a big focus on dwarf birch, which is a nationally scarce species. It’s a shrub and it grows on mountains in Scotland and one or two other isolated places. It’s been declining for many centuries. We’ve done work to understand the genetic variability found in populations of dwarf birch, and where it might be good to plant different genotypes of dwarf birch in the future, and which populations would benefit from assisted gene flow. So that’s much more of a conservation population genetics type study that we’ve been doing on dwarf birch.

FLG: How can all this research in trees help with climate change and sustainability?

Richard: Obviously, there’s a massive emphasis at the moment on tree planting not only in the UK, but around the world to sequester carbon. And of course, we need a diversity of tree species to be able to plant in new woodlands. But if pests and pathogens are decreasing the palette of tree species that we have available for planting that means that we end up planting woodlands that are less resilient, less diverse, less able to support a range of invertebrates and other biodiversity. So, if we can tackle these tree health issues and if we can keep planting ash and maybe even bring back Elm, so that we can be planting Elm as well, we just end up with a more diverse, more resilient woodland in the long run. And of course, every time a new pandemic sweeps through, a whole load of carbon that’s fixed in trees becomes released because the trees die, and they rot or get burned. This is really key to try and sequester carbon and try and keep carbon sequestered that has already been sequestered.

FLG: Kew launched a project called the UK National Tree Seed Project in 2013. What was the ultimate goal of this project? How will it help in terms of conservation?

Richard: Yeah, so that was a major project. It involved seed banking seeds from native UK tree species all across the country. Trees were sampled across their full range, in every native seed zone, across the country, and at different altitudes as well, and then they were banked in the Millennium Seed Bank at Wakehurst. That has created a store of the genetic diversity of UK tree species. It’s something that we can hopefully go back to, if we need to, after a pandemic. But also, it’s an incredibly valuable resource for someone like me who’s doing genomic research, because every so often we have to take seeds out to check they can germinate. And so, what we’re doing now is starting to do genomic research on those seedlings from these collections in order to try to understand signatures of local adaptation across the country in these different trees. If we can do genome environment association studies on the seed collections, then we can start to make suggestions about what seeds would be best to plant in different areas of the country. So, at the moment, we have quite a crude system of deciding what to plant where we have the country divided up into different seed zones. If you’re someone with a grant from the government to plant a new woodland, you have to plant seeds that come from your seed zone or from one of the neighbouring ones. That’s how we’re trying to ensure local adaptation. But of course, that’s a very crude measure. Using genomics, we could actually be saying, ‘Well, this seed source is very well adapted for this type of environment and this one for this type of environment’. We could have a much finer and more detailed picture of what needs to be planted there. Or indeed, if there’s very little local adaptation, then we could say, ‘Well, it doesn’t really matter where you source your seeds from, you can get them from anywhere in the country, and plant them’. Then it becomes less restricted. Also, we can start to factor in climate change and say, ‘Well, let’s predict what the climate will be in 20 years time and let’s plant seeds with that in mind, and include that in our models’. So, we’re hoping that this research will end up making our woodlands more productive and more able to sequester carbon rapidly.

FLG: Aside from your research in trees, you also investigate food insecurity in Ethiopia. Would you be able to expand on what you’re doing over there?

Richard: Yeah, so I’m collaborating with a much larger consortium that involves Royal Botanic Gardens Kew, and University of Greenwich, and many different institutions in Ethiopia. We’re all working together to try to understand genetic signatures of local adaptation in crops grown by farmers in the Southern Highlands of Ethiopia. It’s a really fascinating area, you have huge altitudinal gradients and highly productive farms. This part of Ethiopia didn’t have the big famines that made the headlines back in the 1980s because they have very resilient food systems. We’re trying to look for signatures of local adaptation in the crops and the different plants that are being grown by farmers to try to help understand what should be planted where and how that should change under climate change. One of the major focuses we have, and this is led by a Research Fellow called James Borrell, is a plant called enset (Ensete ventricosum), which is a massive plant relative to the banana that’s grown not for its fruits, but for its stem. The stem is processed and eaten. We’re doing research on local adaptation in that, how many different varieties there are and how planting can be optimised for that particular crop which supports over 20 million people.

FLG: What have been some of the key findings so far?

Richard: We are at quite an early stage with this. In terms of the work on enset, we found that there are lots of different lineages. But sometimes it’s hard to tell from the names that are given, which one is which. So, there are some varieties that have different names but turn out to be genetically very similar. Then, there are other things that have very similar names, which turn out to be genetically different. So that’s been very interesting. Of course, part of this is due to the highly local nature of planting for some of these strains. Going forward, we want to look at things like disease resistance in enset. And as I said the degree to which it’s adapted to the altitude. But we don’t have any results on that yet, we have the data that we’re analysing but don’t yet have results. So, watch this space!

FLG: How are you collaborating with the researchers and the local farmers in Ethiopia to conduct this research?

Richard: Yeah, we have really, really strong collaborations with universities in Ethiopia, and really good relationships with individual academics out there. They have some really good collections of different races and strains of the different crops that are being grown. So, we’re helping with genomics to try and ‘genomify’ this research. We go around to local farmers with them and interview the local farmers about what they’re growing and ask them the names of the different strains of the different crops that they’re growing and try and understand whether they’ve bought the seed commercially or whether they produced it themselves. So, it’s really, really fascinating work. And, as I say, highly collaborative with Ethiopian farmers and academics.

FLG: Big, big team effort.

Richard: It is a huge team effort.

FLG: What does the future of this research look like in terms of your research on trees?

Richard: Well, unfortunately, it’s a growth area, because there are so many tree diseases, but also because we do now have the ability to do something about them through genomics. I’m quite optimistic that, in general, there is a lot of potential to improve our trees in terms of their productivity and their ability to fix carbon. If you just think about a crop like wheat, and you think about the wild relatives of wheat that our wheat came from, and then the extent to which we’ve been able to improve the productivity of wheat over the years through breeding. Then, you compare that with trees, which are essentially undomesticated, we’ve not really done any breeding with them, especially our native broadleaf trees. Then I think, if we’ve been able to do it for wheat, what might we be able to do for trees if we really start to put effort into tree breeding and accelerate it with genomic methods. Now, I’m not talking about doing GM, I’m just talking about traditional breeding programmes, but using genetic methods to know what’s out there and to select the trees at a very early stage. I’m very optimistic that we’ll be able to improve the growth rates of trees and the growth form of trees, and the speed at which they can fix carbon, and maybe even the size to which they can grow. If we could do these things, then we could really have much faster carbon fixation and woodland growth and timber production, and just be more sustainable in the way we use natural resources.

FLG: Thank you so much for joining me today, Richard. I feel with genomics, we often look at it from the human health aspect. But I think, obviously, our environment around us is so important and obviously affects us and I think trees are such a big part of our environment. And this research is really, really important to understand that a bit more and to help with things like climate change and sustainability. So, thank you so much for sharing your insights and the great work that you’re doing as well.

Richard: Pleasure. Thanks for having me.

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