Can Soil Microbes Protect Plants from Herbivore Attack?

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00:00:12.29 Imagine you’re this deer,
00:00:14.20 chomping away on some tasty vegetation
00:00:17.16 when suddenly a wolf, one of your most dangerous predators,
00:00:20.00 shows up.
00:00:21.08 What do you do?
00:00:22.24 You probably run for your life.
00:00:24.23 But what if, instead, you are one of these goldenrod plants,
00:00:27.21 for which the presence of this deer
00:00:29.22 probably presents an equally dire scenario.
00:00:32.07 You can’t run away because you’re literally rooted into the ground.
00:00:36.26 One of the things that I find most fascinating about plants
00:00:39.26 is that, unlike most animals,
00:00:41.09 they can’t simply run away from their problems,
00:00:44.03 like these hungry deer.
00:00:46.01 And if you zoom in even closer,
00:00:48.01 you’ll see that this goldenrod plant
00:00:50.20 also has to deal with herbivores on a smaller scale,
00:00:53.10 like these Trirhabda beetle larvae
00:00:55.07 that are crawling around on this plant and eating it alive.
00:00:58.17 While we can swat away mosquitoes and other insects that are biting us,
00:01:03.07 plants don’t have that type of mobility either.
00:01:05.29 However, this isn’t to say that plants are helpless.
00:01:09.13 Because they can’t move, plants have evolved a variety of interesting mechanisms
00:01:13.29 to protect their tissues against herbivores.
00:01:17.08 These include physical defenses, like these giant thorns on a honey locust tree,
00:01:21.27 which would be pretty effective against our friend, the deer,
00:01:25.19 as well as smaller scale spikes called trichomes,
00:01:28.19 which would be more effective against these beetle larvae.
00:01:32.16 But you probably know that not all plants are spiky and spiny,
00:01:36.19 but it doesn’t mean that they’re not defended.
00:01:39.18 One classic example is this infamously innocuous looking plant,
00:01:42.13 poison ivy,
00:01:44.03 which contains the toxic compound urushiol in its leaves,
00:01:47.00 which causes an allergic skin reaction in many people.
00:01:50.28 This is an example of a chemical defense.
00:01:54.22 Plants are really masterful chemists
00:01:56.21 and can produce all sorts of toxic and anti-digestive compounds
00:02:00.04 to protect their tissues from herbivores.
00:02:02.20 These include some compounds that you may have heard of
00:02:05.07 or may even like,
00:02:07.11 such as nicotine, caffeine, or tannins,
00:02:09.27 which give wines through astringent taste.
00:02:12.15 So, why aren’t all plants covered in spikes
00:02:14.13 and full of super toxic chemicals?
00:02:17.14 Well, plants need to balance their investments in defense
00:02:20.06 with their needs to grow and reproduce;
00:02:22.16 in other words, if they’re using all of their nutrients
00:02:24.16 to grow giant spikes,
00:02:26.13 that’s less that they can put towards growing fast
00:02:29.00 and outcompeting neighboring plants.
00:02:31.20 As a result, there’s lots of variation in plant defenses
00:02:34.27 both between and within species.
00:02:38.11 It’s this variation within species
00:02:40.29 that I’m particularly interested in.
00:02:44.09 One of the larger questions that’s shaping my research is,
00:02:47.20 what are the important factors that are determining plants’ resistance to herbivory?
00:02:52.04 In other words, why are the goldenrod plants in this patch on the left
00:02:55.28 nearly free of herbivores,
00:02:57.22 whereas the ones on the pa…
00:02:59.06 in the patch on the right are being totally decimated
00:03:01.12 by these Trirhabda beetle larvae.
00:03:04.00 This isn’t just an interesting question for a biologist like me,
00:03:07.25 but it can have really important implications in agriculture.
00:03:11.17 It’s estimated that every year 10-20% of potential crop yields
00:03:15.13 are lost due to insect pest damage,
00:03:18.00 so understanding why these corn plants in the field on the left
00:03:22.07 are looking really healthy and vigorous
00:03:24.04 whereas the ones on the right are suffering severely from stem borer damage
00:03:26.22 is important information that can help us
00:03:30.00 develop better pest management strategies
00:03:31.23 and improve food security.
00:03:34.21 But let’s come back to our patches of goldenrod,
00:03:36.29 because that’s what I like to study,
00:03:39.03 and I think that we can actually learn a lot about
00:03:41.24 how to improve the pest resistance of our crops
00:03:43.21 by studying non-crop models like goldenrod
00:03:46.22 and studying natural variation in herbivory.
00:03:49.23 One way to go about investigating the important factors
00:03:52.09 that influence plants’ resistance to herbivores
00:03:54.29 is to find environments where there’s a lot of variation in herbivory
00:03:58.15 — that is, places where we might find patches
00:04:00.22 that look like these two shown here —
00:04:03.00 and then compare them.
00:04:05.29 One place where we might expect to see
00:04:08.10 really big differences in the expression of plant defenses
00:04:10.05 is over the course of ecological succession,
00:04:13.04 which is the process through which the structure of communities
00:04:15.24 changes over time.
00:04:17.23 These changes are particularly interesting and dynamic
00:04:21.26 after a disturbance to the community,
00:04:23.26 for example, when a forest is cut down, tilled,
00:04:26.13 and used for agriculture.
00:04:28.26 If this field was left abandoned,
00:04:30.27 it would quickly become colonized by fast-growing, weedy plants,
00:04:34.28 and after a couple years might look something like this.
00:04:38.21 But eventually it turns back into a forest.
00:04:42.09 Succession creates a really nice framework
00:04:44.17 for studying plant-herbivore interactions
00:04:46.12 because the dynamic shifts in communities,
00:04:48.18 as well as abiotic environments,
00:04:50.24 create places where we might find plants on opposite ends of the spectrum
00:04:55.01 of this aforementioned growth-defense trade-off.
00:04:58.14 Typically, after a disturbance in areas
00:05:01.03 colonized by fast-growing, opportunistic plant species
00:05:03.12 that tend to not be very well defended,
00:05:06.04 but are then over time gradually replaced
00:05:08.20 by slower growing but more strongly defended plant species.
00:05:13.12 This species pattern of herbivore resistance
00:05:15.11 has been really widely studied over succession
00:05:17.23 and inspired a lot of classic plant defense theory.
00:05:20.23 But the herbivore resistance of individual plant species
00:05:24.05 over succession hasn’t been studied in the same way,
00:05:26.23 even though some species,
00:05:28.09 such as goldenrods,
00:05:29.26 persist over a wide range of successional stages.
00:05:33.21 For instance, goldenrod is one of the earliest colonizers after agriculture,
00:05:37.16 typically coming in within the first year
00:05:40.03 of agricultural abandonment,
00:05:41.08 but continues to persist and dominate
00:05:44.02 even as woody plants are starting to enter the scene.
00:05:47.10 We might expect individual plant species like goldenrods
00:05:50.18 to follow the same community level patterns of herbivore resistance —
00:05:55.03 that is, being relatively weakly defended early on in succession,
00:05:58.05 resulting in a lot of herbivory,
00:06:00.16 but being more strongly defended in later succession,
00:06:03.12 resulting in low levels of herbivory.
00:06:08.07 Thus, the research question
00:06:09.26 that was motivating my dissertation was,
00:06:11.26 how does the herbivore resistance of a single plant species, goldenrod,
00:06:16.07 change over succession?
00:06:18.28 The plant species on which I’m focusing
00:06:20.20 is the tall goldenrod, Solidago altissima,
00:06:23.24 which is a common perennial aster
00:06:26.07 native to northeastern North America,
00:06:28.01 although it’s become widely invasive across Asia and Europe.
00:06:31.27 In Upstate New York, where I studied goldenrod,
00:06:34.15 it’s known to interact with over 100 different insect herbivores,
00:06:38.02 but one of the most damaging ones by far
00:06:40.01 was this goldenrod leaf beetle called Trirhabda virgata,
00:06:43.22 which consumes goldenrod in both its larval and adult stages.
00:06:48.25 Thus, most of my work has focused on the interaction
00:06:50.26 just between goldenrod and Trirhabda.
00:06:55.24 In order to study changes in goldenrod’s herbivore resistance phenotypes
00:07:00.04 over succession,
00:07:01.09 I’m making use of this large-scale successional field experiment
00:07:04.14 that we have set up up in Upstate New York.
00:07:07.26 In this experiment, we have different plots
00:07:11.18 that go through this 9-year successional sequence,
00:07:13.11 in which we grow corn conventionally for 3 years,
00:07:16.18 which is our agriculture, or our disturbance,
00:07:19.17 and then we leave the fields fallow for 6 years,
00:07:21.15 which is where we’re able to observe succession.
00:07:24.20 And these plots are replicated and duplicate
00:07:27.02 and staggered chronologically
00:07:28.18 so that at any given time
00:07:31.03 we have two plots representing each successional year.
00:07:34.08 This is really nice,
00:07:36.00 because we can go in at one time and sample across all these different years of succession
00:07:39.29 at the same site,
00:07:41.22 so we can control for other potentially confounding
00:07:43.19 geographic or temporal factors.
00:07:46.20 We also have two older plots that have been fallow since 2002,
00:07:50.15 representing a later stage of succession.
00:07:53.08 So, in my presentation today,
00:07:55.11 you’re going to see these as representing either
00:07:58.05 the 13th, 14th, 15th, or 16th year of succession,
00:08:00.05 depending on when the data were collected.
00:08:03.15 So, we surveyed herbivory on goldenrod plants over succession,
00:08:07.21 and what we found was that there was relatively low levels of herbivory
00:08:12.11 in the… early on in succession,
00:08:14.22 which could be because herbivore populations
00:08:16.28 hadn’t really built up yet.
00:08:19.11 But then in mid-succession,
00:08:21.15 almost every leaf on every goldenrod plant was damaged.
00:08:25.06 And then what was really interesting was that,
00:08:27.16 in late succession, the levels of herbivory dropped.
00:08:30.10 This led us to hypothesize that these goldenrod plants
00:08:34.00 were becoming more resistant to herbivores over succession.
00:08:37.27 So, to investigate this a little bit further,
00:08:40.01 I did some experiments with these Trirhabda beetle larvae.
00:08:44.18 As a measure of feeding preference,
00:08:46.12 I did a feeding choice test,
00:08:47.26 in which I offered a beetle larva discs of leaf tissue
00:08:51.28 punched from plants in early, mid, or late succession,
00:08:55.09 and then after a couple of hours I measured what they ate,
00:08:57.25 and I found that, overall,
00:08:59.06 they tended to avoid feeding on these later succession plants,
00:09:02.07 suggesting that these later succession plants
00:09:03.28 are less attractive as a food source.
00:09:07.17 I also looked at larval performance,
00:09:09.13 or the growth of larvae,
00:09:10.29 feeding on plants from different stages of succession.
00:09:13.27 So, I collected some leaves from plants in different stages of succession,
00:09:18.11 put them in a cup with an herbivore,
00:09:19.22 and after a couple of days I measured how much they ate
00:09:22.17 and how much weight they gained.
00:09:24.08 And I found that, overall, they tended to gain weight less efficiently
00:09:27.22 when they were feeding on these later succession plants,
00:09:29.19 suggesting that these later succession plants
00:09:31.26 are of lesser quality as a food source and are more resistant —
00:09:36.21 potentially, they contain more toxic or anti-digestive plant compounds.
00:09:41.26 Overall, these results suggest that these goldenrod plants
00:09:45.05 are becoming more resistant to herbivores over succession.
00:09:47.27 So, what we want to know is,
00:09:49.21 how are they becoming more resistant over succession?
00:09:53.06 There are two ways through which the average phenotype
00:09:56.20 of a population can change.
00:09:58.06 The first is rapid microevolution,
00:09:59.29 or changes in the frequency of plant genotypes,
00:10:03.08 which we believe is one of the major ways
00:10:05.11 through which these plants are becoming more resistant.
00:10:07.22 In order to test this,
00:10:09.11 we collected plant genotypes or plant lines
00:10:11.19 from different stages of succession,
00:10:13.26 grew them up in a common garden in the greenhouse,
00:10:16.10 and then compared their resistance to these Trirhabda beetles.
00:10:20.18 And overall, what we found was that these later succession genotypes
00:10:23.24 tended to be more resistant than their earlier succession counterparts,
00:10:27.07 suggesting that there might be some selection
00:10:29.21 for more resistant goldenrod genotypes over succession.
00:10:33.16 The second mechanism,
00:10:36.04 which I’m going to focus on primarily in this presentation,
00:10:38.16 is phenotypic plasticity,
00:10:41.10 or changes in the plant’s herbivore resistance
00:10:43.28 due to environmental changes over succession.
00:10:47.01 So, there’s a lot of things that change over succession,
00:10:49.18 like levels of soil nutrients
00:10:51.20 and changes in the composition of the plant communities,
00:10:54.28 but what I’m focused on here is microbe-mediated phenotypic plasticity.
00:11:01.13 We hypothesized that there would be changes
00:11:03.25 in the soil microbial communities
00:11:05.20 that these goldenrod plants are interacting with over succession,
00:11:08.23 which would, through interacting with the plant,
00:11:11.02 alter the plant’s chemical defenses.
00:11:13.27 Microbes, like plants, are really impressive chemists
00:11:16.11 and can produce all sorts of different compounds
00:11:19.00 and hormones
00:11:20.04 that can interact with the plant
00:11:22.27 and alter the plant’s metabolism,
00:11:24.06 so we predicted that they would alter the plant’s chemical defenses,
00:11:27.13 which would then alter their interactions
00:11:30.19 with herbivores like Trirhabda.
00:11:32.29 So, the first thing that I had to do is see
00:11:36.07 if these soil microbial communities that these goldenrod plants
00:11:38.13 were interacting with
00:11:40.01 actually changed over succession.
00:11:42.11 So, I did some surveys of the rhizosphere soil communities
00:11:45.20 of goldenrod plants over succession.
00:11:48.22 The rhizosphere soil is just the soil
00:11:51.11 that’s immediately surrounding the roots of the plant
00:11:53.05 and most likely to be interacting with the plant.
00:11:56.02 And then I characterized them by sequencing DNA barcoding regions
00:12:00.28 of these microbes that are commonly used
00:12:04.02 to identify bacteria and fungi.
00:12:06.22 So, visualizing the communities of microbes
00:12:09.15 is a bit complicated because they’re super diverse,
00:12:12.03 with thousands of different taxa.
00:12:14.08 Scientists often use a technique known as ordination
00:12:17.18 to broadly capture the differences between these different microbial communities
00:12:22.00 and see, overall,
00:12:24.11 which ones are more similar or more different.
00:12:26.26 So, I’m just going to briefly walk you through one of these ordination plots.
00:12:31.04 So, first off, you don’t need to worry about
00:12:34.10 what these different axis labels mean
00:12:36.07 in order to interpret the data.
00:12:38.22 In this space, I’m going to be plotting
00:12:40.27 these different rhizosphere bacterial communities of these different goldenrod plants,
00:12:44.13 and they’re going to get…
00:12:46.17 there are going to be points that are getting increasingly dark purple
00:12:49.15 with increasing successional age.
00:12:51.11 So, this point here, this really light purple one,
00:12:54.14 is going to be the rhizosphere bacterial community
00:12:57.18 of a goldenrod plant from early succession,
00:13:00.21 this kind of medium purple would be one from mid succession,
00:13:04.15 and then this dark purple one would be
00:13:07.00 the community of a plant from late succession.
00:13:10.22 And how you can interpret these types of plots
00:13:13.08 is that points that are located in closer spatial proximity
00:13:16.19 mean that the communities are compositionally more similar,
00:13:20.02 whereas points that are far apart
00:13:23.03 mean that the communities are more different.
00:13:24.28 So, in this plot here,
00:13:27.03 the mid and late succession communities
00:13:29.21 are compositionally similar,
00:13:30.27 whereas the early succession one is more different.
00:13:35.27 So, in terms of succession,
00:13:37.19 we might expect that the communities separated
00:13:40.01 by the most successional time
00:13:42.02 would be the most compositionally different,
00:13:44.15 in which case we would see that the early and late succession communities
00:13:48.02 would be far apart,
00:13:50.04 and the mid-succession ones would be somewhere in the middle,
00:13:52.09 which would look something like this.
00:13:56.00 So, this is what our data actually look like,
00:13:57.24 which is kind of a lot to look at,
00:14:00.12 but you can kind of tell that these dark, late succession microbial communities
00:14:04.24 tend to be clustered towards the top,
00:14:06.14 the early succession ones are kind of at the bottom,
00:14:09.07 and the mid succession ones are scattered throughout the middle,
00:14:12.18 illustrating a shift in bacterial community composition
00:14:16.03 over successional time.
00:14:19.13 We also surveyed fungi in the rhizosphere,
00:14:21.20 and we found a similar pattern,
00:14:23.24 where there was a shift in the composition of these microbial communities
00:14:28.12 over successional time.
00:14:30.23 Overall, these results suggest that the communities of microbes
00:14:35.03 that these goldenrod plants are interacting with
00:14:37.17 change over succession.
00:14:39.08 So, what we want to know is
00:14:41.08 if these soil microbial shifts were mediating, to any extent,
00:14:44.13 this increase in herbivore resistance that we observed in the field
00:14:47.20 over succession.
00:14:49.23 So, in order to test this,
00:14:51.19 I did a soil microbiome transplant experiment,
00:14:53.20 in which I collected soil microbiomes,
00:14:55.28 just as little bits of field soil,
00:14:57.28 from different stages of succession
00:14:59.21 — early, mid, and late —
00:15:02.10 and then I used these to directly inoculate sterilized potting media
00:15:05.12 in the greenhouse,
00:15:07.06 planted goldenrods in these mesocosms,
00:15:09.17 grew them up,
00:15:11.02 and then compared their herbivore resistance
00:15:13.14 to these Trirhabda beetles.
00:15:15.28 Once again, as a measure of herbivore resistance,
00:15:18.22 I looked at feeding preference.
00:15:21.04 So, I offered a Trirhabda beetle discs of leaf tissue
00:15:24.12 punched from plants inoculated
00:15:27.03 with early, mid, or late succession soil microbial communities.
00:15:30.08 So, within each test all these plants were genetically identical.
00:15:33.27 The only thing that was different was the microbial community
00:15:36.19 with which they were inoculated.
00:15:39.06 And after a couple of hours,
00:15:40.27 I measured what they ate,
00:15:42.24 and overall I found that they tended to prefer eating plants
00:15:46.12 inoculated with the earliest succession soil microbiomes,
00:15:49.15 whereas they tended to avoid eating the ones
00:15:51.22 that were grown in the late succession soil microbiomes.
00:15:55.04 This was super exciting because it suggests
00:15:57.26 not only that the soil microbiome alone
00:16:01.10 can affect plants interactions with herbivores,
00:16:02.29 but it also nearly parallels these patterns of herbivore resistance
00:16:06.13 that we observed in the field,
00:16:08.03 with the later succession plants
00:16:10.18 being more resistant to herbivores
00:16:12.07 and experiencing really low levels of herbivory.
00:16:14.22 This suggests that these soil microbial shifts
00:16:17.09 could be playing a major role in mediating
00:16:20.02 this increase in herbivore resistance.
00:16:22.29 So, in summary, the herbivore resistance of a plant, goldenrod,
00:16:28.00 increases over succession,
00:16:30.13 and at the same time the soil microbial communities
00:16:32.28 that these goldenrod plants are interacting with
00:16:35.18 also shifts over succession.
00:16:37.07 And through this transplant experiment,
00:16:39.21 we were able to show that these soil microbial shifts
00:16:42.10 at least have the potential to mediate this increase
00:16:44.17 in herbivore resistance
00:16:46.20 that we observed in the field.
00:16:48.20 While I didn’t focus on it in this presentation,
00:16:51.03 we’ve also seen genotypic shifts in the plant populations,
00:16:54.05 where late succession plant genotypes
00:16:56.16 tend to be more resistant than their earlier succession counterparts.
00:17:01.01 Overall, it was super exciting to see that
00:17:04.00 these late succession soil microbial communities
00:17:06.11 seem to be conferring herbivore resistance to goldenrod plants.
00:17:09.09 So, one of the things that we were wondering was
00:17:12.02 if these late succession soil microbial communities
00:17:14.05 could also improve the herbivore resistance of other plant species,
00:17:17.14 especially crop species that have really major insect pest problems.
00:17:23.06 We repeated some of these soil microbiome transplant experiments
00:17:26.15 with other plant species:
00:17:28.15 tomato, cucumber, corn, and lettuce.
00:17:31.16 And while it varied from plant species to plant species,
00:17:34.23 typically what we found was that these later succession soil microbiomes
00:17:39.15 generally conferred greater resistance to a caterpillar pest,
00:17:42.27 Trichoplusia ni,
00:17:44.12 especially compared to plants that were grown
00:17:47.17 in agricultural soil microbiomes.
00:17:50.07 This suggests that this phenomenon that we discovered in goldenrod
00:17:54.00 may have applications in agriculture.
00:17:58.09 In conclusion, we’ve seen that soil microbiomes
00:18:01.01 can affect plants’ resistance to herbivores,
00:18:03.08 and specifically, changes in soil microbial communities over succession
00:18:07.20 can increase plants resistance to herbivores.
00:18:11.19 This suggests that soils could be potential sources
00:18:14.02 of beneficial soil microbial communities
00:18:16.21 that could be used to improve plants’ resistance
00:18:19.17 to insect pests.
00:18:22.20 So, with that, I’d like to thank many of the people
00:18:25.07 who have contributed to this project,
00:18:27.00 particularly people in the Kessler and Kao-Kniffin labs,
00:18:30.08 as well as my various funding sources.
00:18:33.01 And thank you for listening.

This Talk

Speaker: Mia Howard

Audience:

Student
Educators of Adv. Undergrad / Grad
Researcher
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Recorded: June 2021

Talk Overview

Unlike most animals, plants don’t have the option to run away when something is trying to eat them. Instead, they develop all kinds of chemical and structural defenses. But these defenses can be energetically costly, and plants’ ability to defend themselves can change over time and with the environment. In her Share Your Research Talk, Dr. Mia Howard discusses how soil microbes can influence defensive traits in goldenrod (Solidago altissima) at various stages of succession. Her work reveals that microbial communities from late succession soils can increase plant resistance to herbivory, and may even make plants less vulnerable to pests.

Speaker Bio

Mia Howard

Mia Howard is an ecologist interested in soil microbes and plant-herbivore interactions. She completed her doctoral research at Cornell University, where she studied the chemical ecology of plant-microbe-insect interactions in native goldenrod (Solidago altissima), and is currently a postdoctoral research fellow at Indiana University. Continue Reading

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