Daily Factoid: Some insects parasitise plants

In a brilliant bit of parasitism, galling insects drill into plants and affect their metabolism and development in such a way that galls form. The exact molecular mechanisms for this are still largely unknown, but what is known is that these galls are highly-advantageous for the insects. They can take various forms, from being mere modifications of the plant’s nutrient production (inducing greater protein and sugar production for the insect to feed on), to being local growths of nutrient-rich plant tissues on which the insect can munch, to full-blown houses for the insect to live in.

Other insects are leaf-miners, and some of these insects also have the ability to modify the plant’s development. Next autumn, observe the trees with yellow leaves about to drop off. Some of them might have green “islands” on them – areas that are still photosynthetically active even though the rest of the leaf is ageing and dying.

Biochemical analyses of both leaf mines and galls show higher levels of cytokinins, plant hormones that inhibit ageing, maintain chlorophyll, and enhance nutrient release. In other words, the green mined areas are much more nutritious than the rest of the leaf. Like galls, they’re induced by the leaf-mining insects to get an easy source of food – and at a critical time of the year, right before winter.

What’s as interesting as this modification of plant structure by parasitic insects (which is, in principle, similar to behavioural modifications by animal parasites), many studies suggest that the involved cytokinins are not of plant origin, but injected directly by the insects. Going even deeper, the cytokinins injected by the insects aren’t produced by the insects, but by bacterial symbionts. Draw that on a flowchart to see how cool this is: it’s a triple-layered interaction that’s been most likely moulded by millions of years of coevolution.

Further Reading:

General:

The evolution and adaptive significance of the leaf-mining habit

Geometrical Games between a Host and a Parasitoid

Cytokinins and insect galls

Galls:

Manipulation of the phenolic chemistry of willows by gall-inducing sawflies

Mines:

Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests

Cytokinins:

Extracellular Invertase Is an Essential Component of Cytokinin-Mediated Delay of Senescence

Pathological hormone imbalances

Top Research of 2012: Botany

Jump to: Arthropods; Developmental Biology; Ecology; Environmental; Evolution; Geology; Historical Geology; Human Evolution; Palaeontology; Zoology.

My top 10 picks for botanical research this year. I’m not a botanist, and although I am fascinated by plant physiology, I’m not intellectually able to keep up with that research. So I only really follow plant evolution, palaeobotany, and plant-arthropod interactions; I have tried to make the list more varied though. Picks and rankings are subjective, based on a master list of 17 papers. [OA] indicates an open-access paper.

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10. Broad Phylogenomic Sampling and the Sister Lineage of Land Plants. [OA]

Land plants (Embryophyta) are highly-specialised streptophyte green algae. Of the other streptophyte groups, three are variably recovered as the sister group to the land plants, the results depending on the genes and methods used, and none ending up with truly rigorous support: the Charales, the Coleochaetales, and the Zygnematales (pond scum). The Charales (stoneworts) are the ones commonly depicted in textbooks and have always gained the most support. This paper may change our view on things: it uses a large dataset of 160 phylogenetically-significant genes, and gets perfect support values for a Zygnematales+Embryophyta clade. This has numerous implications, chief of which is that multicellularity is a convergent land plant innovation rather than a condition inherited from an ancestor (as would be the scenario if Charales are the sister).

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9. Plant UVR8 Photoreceptor Senses UV-B by Tryptophan-Mediated Disruption of Cross-Dimer Salt Bridges.

This paper studies the molecular basis for UV light detection (280-320 nm) in plants, by looking at the reactions of UVR8, a photoreceptor known to react to UV light. Christie et al. went classical in this paper: they used crystallographic methods to elucidate UVR8′s structure, best summarised as a doughnut; then they used targeted mutations to find out how the protein works. When inert, it’s found as a dimer: two doughnuts connected by bridges. When UV light shines on the plant, these bridges break due to electrons getting excited. The single doughnut then binds to another protein, COP1, to complete the reaction.

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8. Phylogenetic niche conservatism in C4 grasses.

I’ve written an overview of C4 photosynthesis, so refer to that post for necessary background. This paper analyses various traits in grasses of the Chloridoideae and Panicoideae, grasses in which C4 photosynthesis is dominant (in the phylogeny above, yellow indicates C3, all other colours are types of C4). It finds that the evolution of these traits, as well as ecological preferences, are determined not by the evolution of C4 photosynthesis, but by phylogeny. In other words, it’s the ancestry that counts. This in turn has implications about how we should treat C4 photosynthesis: there is a tendency to lump C4 plants together as one functional group, regardless of phylogeny. This finding says we are better off sticking to phylogenetic lumping, since there is clear niche conservatism: C4 photosynthesis doesn’t determine the ecology of these plants. Ancestry does, and C4 photosynthesis just tags along.

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7. A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution. [OA]

This paper presents a cool hypothesis for a contributing factor to the great angiosperm radiation of the Cretaceous: leaf vein density (D_v in the above diagram) as a key feature. This is an observation in the fossil record, that the density of the veins increases in two bursts, once in the initial angiosperm radiation (100 Ma) and another time at 65 Ma to reach today’s levels. The greater vein density leads to vastly improved gas exchange rates, which would have provided them with a distinct advantage as the CO₂ levels decreased in the Cretaceous, allowing them to more easily outcompete the conifers and other land plants.

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6. Widespread impact of horizontal gene transfer on plant colonization of land. [OA]

This genomic analysis of a moss, Physcomitrella patens, finds that it has 57 nuclear gene families by horizontal gene transfer from bacteria, fungi, or viruses. 18 of them are inherited ancestrally; 18 of them are recent acquisitions; and 15 of them are also found in more derived land plants, passed on from the last common ancestor with mosses. To put these numbers into perspective, the functions of the acquired genes are essential, involved in defence and stress tolerance, hormone biosynthesis, and even DNA repair. The picture painted by these facts is one of a harsh environment that early land plants had to colonise, in which UV radiation was rampant and the ground was inhospitable; these genes enabled the early mosses to survive by helping DNA stability in early mosses (later plants got yellow pollen, the yellow pigment serving as a UV shield), and numerous stress tolerance mechanisms and development helpers to keep them surviving in the harsh environment.

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5. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior.

This is some pretty cool research from an ecological and from a plant-insect interaction perspective. The study finds that plant defence systems can be synchronised with insect feeding times; at least it is so in the case of the caterpillar of Trichoplusia ni and the Arabidopsis weed this experiment was done on. The synchronisation is achieved not by detecting the caterpillar, but by circadian rhythms – when raised on the same day/night cycle, the plant’s defence system will adjust to be active at the same time as the caterpillar is active. When circadian mechanisms are interrupted or the hormone jasmonate’s production is deficient, then the synchronisation gets thrown off and the plant experiences much higher herbivory levels and are thus at a physiological disadvantage. I’m interested in seeing how this plays out in nature with day-active vs. night-active insects.

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4. Cyanophora paradoxa Genome Elucidates Origin of Photosynthesis in Algae and Plants.

This paper reports the draft nuclear genome of the basal glaucophyte alga Cyanophora paradoxa. The most significant result is evidence for the monophyly of the Plantae, as even the untypical plastid of the glaucophytes appears to be homologous with that of the rhodophytes and green algae (together, these three groups make up the Plantae). The data gathered from the genome says that 274 of the alga’s proteins were transferred from endosymbiotic cyanobacteria, and that 444 gene families were transferred by horizontal gene transfer from other bacteria. Many of these proteins and genes are involved in photosynthesis and associated processes, as well as plastid integration, meaning that we now have more light shone on how built-in photosynthesis in plants first evolved.

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3. Oldest known mosses discovered in Mississippian (late Visean) strata of Germany.

Mosses are expected to be one of the earliest plants to have evolved on land, but their early fossil record has been severely lacking because of their very low preservation potential. This paper describes the oldest mosses to date, which grew in the tropical forests of the German Carboniferous. Older ones are still to be expected, but their lack is merely an example of an expected inadequacy in the fossil record.

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2. Underground leaves of Philcoxia trap and digest nematodes.

I admittedly include this so high up because of the coolness factor, but it does bring up deeper issues. But first, the cool stuff: the plant has sticky leaves that grow underground. Nematodes stick to them, and the plant digests them. In other words, this is a carnivorous plant, and it uses a completely novel way to capture its food. The deeper ecological and evolutionary issue to be brought up is about how such a unique strategy can evolve.The plant grows in a region with one of the poorest soils of the world, the Brazilian Cerrado. So it could be that the evolution of carnivory is instigated by soil nutrient deficiencies, and so they eat animals in order to get those critical nutrients.

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1. Rise to dominance of angiosperm pioneers in European Cretaceous environments.

This paper reviews the early record of angiosperm fossils from Europe to propose a temporal framework for their megadiversification in the Cretaceous in which they outcompeted the conifers and other land plants. The scenario Coiffard et al. synchs up with the view from the North American record, so it can be viewed as reliable. The scenario has three bursts of diversification into new habitats. From the abstract: “(i) Barremian (ca. 130–125 Ma) freshwater lake-related wetlands; (ii) Aptian–Albian (ca. 125–100 Ma) understory floodplains (excluding levees and back swamps); and (iii) Cenomanian–Campanian (ca. 100–84 Ma) natural levees, back swamps, and coastal swamps.”

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Jump to: Arthropods; Developmental Biology; Ecology; Environmental; Evolution; Geology; Historical Geology; Human Evolution; Palaeontology; Zoology.

Zoology

C4 Photosynthesis

C4 plants are plants that undergo a specialised extrametabolic pathway, the C4 cycle, in which CO₂ is transferred from mesophyll cells to a special ring of bundle sheath cells by a pump. CO₂ gets dissolved by carbonic anhydrase, forming bicarbonate, which is then fixed with phosphoenolpyruvate carboxylase into C₄ oxaloacetic acid (hence the name), which is then converted to malate. This diffuses to the bundle sheath ring through plasmodesmata, where the CO₂ is set free by decarboxylases, including the all-important RuBisCo (Hatch, 1987). Regular C3 photosynthesis occurs, but under the locally very high CO2 concentrations 3-8x higher than other area of the leaf.

The net result is a minimisation of CO₂ loss through photorespiration, a reduction in use of stomata leading to less water loss through transpiration, and a much higher rate of photosynthesis, at the cost of substantial energy needed to drive the CO₂ pump, energy acquired from sunlight. C4 plants are also more efficient in using nitrogen, since they need to use less enzymes to maintain their higher photosynthetic rates (Pearcy & Ehleringer, 1984).

In practical ecological terms, what those advantages bring is either an ability to grow faster than C3 plants, or an ability to grow in more challenging environments than C3 plants (Hatch, 1987).

The reason why C4 photosynthesis works is the evolutionary history of C3 enzymes, especially the main one, RuBisCo. RuBisCo evolved back in the times when the atmosphere contained very little oxygen and 100x more CO₂ than today (Rye et al., 1995). Therefore, all that C4 photosynthesis does is recreate that atmosphere very locally around the enzyme so that it acts in the environment it evolved to be optimal in, namely an atmosphere with very high CO₂ and low O₂, so that the competitive inhibition of RuBisCo by O₂ is eliminated. For those with engineering experience, C4 photosynthesis works just like a supercharged combustion engine.

Although only 3% of vascular plant species undergo C4 photosynthesis, those plants are responsible for almost a quarter of the photosynthesis that happens on land (Lloyd & Farquhar, 1994). Its evolution is therefore quite an important development not only from a physiological perspective, but also from an ecological one.

C4 metabolism evolved convergently from regular C3 photosynthesis in over 45 land plant families, both monocot and dicot (Sage, 2004), as a result of the steady depletion atmospheric CO₂ levels between 40-15 Ma (Edwards & Smith, 2010). This reduction in CO₂ levels led to inefficiency in carbon uptake in land plants, especially those in warm and arid landscapes (most C4 plants are grasses), providing a strong selective pressure to reduce photorespiration, and by the Pliocene, C4 grasslands had displaced C3 grasslands in lower latitudes. Tropical grasslands and savannahs are dominated by C4 plants, as are many breakfast tables (Sorghum, maize, and sugarcane are all C4). At higher latitudes, the cost of driving the CO₂ pump outweighs the gains: the C4 vs. C3 biogeographical dominance has a threshold defined by temperature (Ehleringer et al., 1997), with C4 plants dominating in warm temperatures and C3s in cold temperatures (the distinction also applies with altitudinal gradients). Other important factors influencing distribution are moisture/precipitation and light intensity.

There are no novel enzymes involved in C4 photosynthesis, it is all achieved using cooption of pre-existing enzymes and changes in their expression patterns causing the enzymes to accumulate to various levels in the mesophyll and bundle sheath cells. These changes are pretty complicated considering that they involve 20-30 unlinked genes (Wyrich et al., 1998) – it’s remarkable that this all evolved convergently so many times. We know of some intermediate species exhibiting some “proto-C4″ characteristics, e.g. several species in the Neurachne, Flaveria, Parthenium, Mollugo, and Alternanthera genera (list just random examples I dug up, there are definitely more!). Xu et al. (2012) show that both C3 and C4 pathways work at the same time in the alga Ulva prolifera.

It’s also worth noting that some unique lineages have managed to make a C4 mechanism that takes place within individual cells rather than in different tissues, see Keeley (1998) for examples.

References:

Edwards EJ & Smith SA. 2010. Phylogenetic analyses reveal the shady history of C4 grasses. PNAS 107, 2532-2537.

Ehleringer JR, Cerling TE & Helliker BR. 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285-299.

Hatch MD. 1987. C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81-106.

Keeley JE. 1998. C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. Oecologia 116, 85-97.

Lloyd J & Farquhar GD. 1994. ¹³C discrimination during CO₂ assimilation by the terrestrial biosphere. Oecologia 99, 201-215.

Pearcy RW & Ehleringer J. 1984. Comparative ecophysiology of C3 and C4 plants. Plant, Cell & Environment 7, 1-13.

Rye R, Kuo PH & Holland HD. 1995. Atmospheric carbon dioxide concentrations before 2.2 billion years ago. Nature 378, 603-605.

Sage RF. 2004. The evolution of C4 photosynthesis. New Phytologist 161, 341-370.

Wyrich R, Dressen U, Brockmann S, Streubel M, Chang C, Qiang D, Paterson AH & Westhoff P. 1998. The molecular basis of C4 photosynthesis in sorghum: isolation, characterization and RFLP mapping of mesophyll- and bundle-sheath-specific cDNAs obtained by differential screening. Plant Molecular Biology 37, 319-335.

Xu J, Fan X, Zhang X, Xu D, Mou S, Cao S, Zheng Z, Miao J & Ye N. 2012. Evidence of Coexistence of C3 and C4 Photosynthetic Pathways in a Green-Tide-Forming Alga, Ulva prolifera. PLoS ONE 7, e37438.

The Origin of Modern Biodiversity: Coevolution of Flowers and Insects

This talk is split into two major parts: the first will look at the general fossil record of insects, and the second will introduce the flowering plants and their interactions with insects.

Terrestrialisation

Due to the inherent time constraints of having to compress what is usually a semester’s worth of knowledge into 4.5 hours, we will now move away from the oceans permanently and look at the rest of the history of life on Earth from only a terrestrial perspective.

To do that, we have to first examine what challenges awaited those few organisms that made the transition to land. Then we will see how they evolved and radiated further, and ending with the most severe mass extinction in the history of life on Earth.

Orchid Sexual Deception

This is a really cool topic that I may write a larger post on sometime in the future. Most orchids are deceptive – i.e. they attract their pollinators by fooling them – but only the most specialised ones are sexual deceivers.

Do Insects Help Seed Dispersal?

The full question here involved insect-flower interactions: insects pollinate, but do they do anything else to help flowers, such as help disperse their seeds. Surprisingly enough, besides exceptional cases, no!

Plant-Arthropod Interactions in the Fossil Record

For a PDF version of this post (better formatted, but no direct links to sources), click here.

Insects are by far the most diverse and numerous of all animal groups and half of them are herbivores. When investigating any ecosystem, it is often wise to just look at plant leaves to get an indication for the diversity of insects there – and obviously, this principle also applies to fossil leaves and fossil insects, as can be seen in the picture below. It is slightly out of date (1998), but is still useful to show that we have these plant-arthropod interactions in the fossil record and for every relevant group. That’s what this post is about.

Animal – Flower Interactions: Pollination

The flower – insect symbiosis is one of the most successful partnerships in biology. I’m talking, of course, about pollination (bee goes in flower to get nectar, picks up pollen on the way, goes to another flower). Flowers often have specialised designs and secrete specific molecules to attract insects. In fact, it is this diversity, and the resulting coevolution of flowers and their insect pollinators, that are key to the angiosperms’ explosive radiation.