Co-evolved plant–animal interactions play a vital role in ecosystem functionality and the persistence of biodiversity. Through natural selection, plants have evolved a variety of dispersal units and mechanisms to overcome mobility issues, the most common of which is to utilize animal agents to facilitate zoochory – dispersal by animals – including endozoochory (inside the gut), epizoochory (outside on fur and feathers) and hoarding (where the squirrel puts his nuts). For example, up to 90% of the plant species in tropical forests disperse seeds via animal agents. Many dry-fruited plants produce appendages (e.g. hooks and hairs) on their reproductive structures to facilitate epizoochory, i.e. external dispersal by animals. Birds and monkeys often act as agents of epizoochory, by carrying infructescences to remote perches to peck or chew on the pulp. The predominant plant dispersal strategy is, however, to produce diaspores that elicit endozoochory, i.e. the consumption and subsequent reappearance of viable seeds by embedding seeds in fleshy pulp. Lush foliage can also attract herbivores to small-fruited herbaceous plants, to promote endozoochory.
A recent paper in Annals of Botany examines why the Chinese raisin tree, Hovenia dulcis, produces enlarged, fleshy peduncles with outer, dry drupes and investigates how this dry-fruited plant disperses its seed. In contrast to previous studies reporting that fleshy appendages entice bird epizoochory, field observations combined with experimental manipulations confirm that H. dulcis peduncles are adapted primarily to achieve mammal endozoochory, with viable seeds being found in the faeces of species such as bears and martens. The germination rate of egested seeds is higher than that of unconsumed seeds, demonstrating a mutualistic association similar in function to production by the plant of fleshy pulp or foliage.
Peduncles elicit large-mammal endozoochory in a dry-fruited plant. Annals of Botany (2013) 112 (1): 85-93. doi: 10.1093/aob/mct096
Plants have evolved a variety of seed dispersal mechanisms to overcome lack of mobility. Many species embed seeds in fleshy pulp to elicit endozoochory, i.e. disseminating seed through the animal gut. In contrast to well-studied fleshy fruited plants, dry-fruited plants may exploit this dispersal mutualism by producing fleshy appendages as a nutritional reward to entice animals to swallow their diaspores, but this has been little studied. In this study, it is hypothesized that these accessory fruits represent. Field observations (focal tree watches, faecal surveys and fruiting phenology) with experimental manipulations (examination of seed germination and feeding trials) were conducted over 2 years in a native population of the raisin tree, Hovenia dulcis, which produces enlarged, twisted brown peduncles with external black seeds, in central China. Birds were not observed to swallow seeds or carry infructescences away during 190 h of focal tree watches. However, H. dulcis seeds were detected in 247 faecal samples, representative of two herbivore and four carnivore mammalian species. Feeding trials revealed that peduncles attracted mammals to consume the entire infructescence, thereby facilitating effective seed dispersal. The germination rate of egested seeds proved higher than that of unconsumed seeds. It was also noted that this mutualism was most vulnerable in degraded forest. Hovenia dulcis peduncle sets are confirmed to adapt primarily to mammalian endozoochory, a mutualistic association similar in function to fleshy pulp or foliage. This demonstrates that plant organ systems can be adapted to unique mutualisms that utilize animal dispersal agents. Such an ecological role has until now been attributed only to bird epizoochory. Future studies should consider more widely the putative role of peduncle sets and mammalian endozoochory as a dispersal mechanism, particularly for those plants that possess relatively large accessory fruits.
Remember the millennium? Maybe you’re too young. (Or possibly you just went to a better party than I did.) Aside from wasting silly amounts of money building stupid domes, one of the better ideas that quite a few people had was the creation of millennium seedbanks and as way of ensuring the prosperity (and full bellies) of future generations by preserving the germplasm of plant species in long term storage. And for flowering plants, that means seeds. But what if, when we really need them at some point in the future, the seeds don’t grow?
Seeds stored for prolonged periods are subjected to severe oxidative damage, caused by the progressive accumulation of reactive oxygen species (ROS) and that loss of seed viability and reduced germination represent the undesired consequences of ageing. Significant factors in seed longevity are the level of DNA damage and the DNA repair response, the amount of non-enzymatic antioxidants and activity of ROS-scavenging enzymes. In order to preserve the high seed viability at the pre-emergence step, both the DNA repair functions and the overall antioxidant activities must be kept at an appropriate level in the embryo. Different DNA repair pathways are activated during the early phase of seed imbibition. The ability to carry out ROS scavenging, expressed as the seed antioxidant potential, is a critical requirement to withstand stress and improve germination. The cell antioxidant systems prevent ROS attack but when ROS production exceeds the capacity of the antioxidant machinery, oxidative injury takes place.
Factors such as temperature and humidity are positively correlated with seed ageing and they must be strictly controlled during seed manipulation for long-term conservation in seed banks. To date, germination tests represent the most reliable method to assess seed viability, although it is a time-consuming and labour-intensive operation. Novel low-cost and equally reliable methods are required, which might speed up the seed viability analysis. Molecular and biochemical markers of seed ageing might be used for these purposes. A deeper understanding of the complex network of molecular events which control seed longevity is, however, required in order to select appropriate markers providing information on deterioration and germination potential of seed stocks collected for bank storage.
A new paper in Annals of Botany investigates reliable markers of seed deterioration. The response to DNA damage induced by artificial ageing was compared in seeds of Silene vulgaris and S. acaulis inhabiting low- and high-altitude locations of Northern Italy. Previous investigations have demonstrated that these species differ in seed longevity, making them useful candidates to assess novel markers of seed deterioration. An in-depth investigation which included ROS accumulation profiles, antioxidant capacity and telomere length was carried out, focusing mainly on dry seeds and seeds subjected to rehydration. A positive impact of the reported results could be envisaged within a relatively short time, since specific suggestions can be derived for improving the rehydration protocol of seeds from a high-altitude location.
DNA profiling, telomere analysis and antioxidant properties as tools for monitoring ex situ seed longevity. (2013) Annals of Botany 111 (5): 987-998. doi: 10.1093/aob/mct058
The germination test currently represents the most used method to assess seed viability in germplasm banks, despite the difficulties caused by the occurrence of seed dormancy. Furthermore, seed longevity can vary considerably across species and populations from different environments, and studies related to the eco-physiological processes underlying such variations are still limited in their depth. The aim of the present work was the identification of reliable molecular markers that might help in monitoring seed deterioration. Dry seeds were subjected to artificial ageing and collected at different time points for molecular/biochemical analyses. DNA damage was measured using the RAPD (random amplified polymorphic DNA) approach while the seed antioxidant profile was obtained using both the DPPH (1,1-diphenyl, 2-picrylhydrazyl) assay and the Folin–Ciocalteu reagent method. Electron paramagnetic resonance (EPR) provided profiles of free radicals. Quantitative real-time polymerase chain reaction (QRT-PCR) was used to assess the expression profiles of the antioxidant genes MT2 (type 2 metallothionein) and SOD (superoxide dismutase). A modified QRT-PCR protocol was used to determine telomere length. The RAPD profiles highlighted different capacities of the two Silene species to overcome DNA damage induced by artificial ageing. The antioxidant profiles of dry and rehydrated seeds revealed that the high-altitude taxon Silene acaulis was characterized by a lower antioxidant specific activity. Significant upregulation of the MT2 and SOD genes was observed only in the rehydrated seeds of the low-altitude species. Rehydration resulted in telomere lengthening in both Silene species. Different seed viability markers have been selected for plant species showing inherent variation of seed longevity. RAPD analysis, quantification of redox activity of non-enzymatic antioxidant compounds and gene expression profiling provide deeper insights to study seed viability during storage. Telomere lengthening is a promising tool to discriminate between short- and long-lived species.
Non-native earthworms have invaded ecosystems around the world but only recently received attention after invading previously earthworm-free habitats in northern North America. Earthworms can affect plants by ingesting seeds and burying them in the soil. The effects, which can be either positive or negative, are expected to become more negative with decreasing seed size.
Because orchids have some of the smallest seeds of any plants, McCormick et al. hypothesized that earthworm consumption would decrease seed viability in these plants and lead to burial of ingested seeds. They used a combination of mesocosms and field measurements to determine whether native and non-native earthworms would affect the seed germination of the North American native orchid Goodyera pubescens by decreasing seed viability through digestion or burial. To determine soil depths at which seed burial would decrease chances of germination, they used field measurements of the abundance of mycorrhizal fungi needed for G. pubescens germination with soil depth.
The researchers found that the combined effects of earthworm ingestion and burial are expected to result in a substantial loss of orchid seeds. Their models estimated that 49% of orchid seeds in mature forests and 68% of those in successional forests would be lost to earthworm ingestion over an average year. The combined effects of earthworm ingestion and burial have the potential to result in a substantial loss of orchid seeds, particularly in successional forests. This effect may slow the ability of orchids to recolonize forests as they proceed through succession. Further testing will determine whether this strong effect of earthworms on G. pubescens viability and germination also applies to other orchid species.
Several ecologically important plant families in Mediterranean biomes have seeds with morphophysiological dormancy. Hidayati et al. study four species of the intractably dormant Australian genus Hibbertia (Dilleniaceae) and find that although they are congeneric, sympatric and produce seeds of identical morphology, they show a remarkable level of variation in dormancy-break and germination requirements. The results have important implications for current classification systems of seed dormancy and highlight the difficulties, and caution required, in extrapolating dormancy requirements in biodiverse regions such as the south-west Australian biodiversity hotspot.
In biology, matters are rarely either good or bad; oftentimes they may be both at once (albeit usually for different organisms). Take for instance hydrogen cyanide, which is widely regarded to be rather bad since it is a potent poison that can kill most living things by ‘interfering’ (that’s a euphemism!) with respiration. However, it seems that cyanide also has a good side. Apart from its role in deterring would-be herbivores, Gavin Flematti et al. propose that it may also act as an important stimulus for the germination of some seeds (Nature Communications). The Australia-based group showed that burning plant material produces glyceronitrile (a cyanohydrin), which releases cyanide upon reaction with water. The cyanide in turn stimulates seed germination – maybe via reactive oxygen production (something else that is usually regarded as ‘bad’) – of Anigozanthos manglesii (which rejoices in the common name of kangaroo paw), and a ‘diverse range of fire-responsive species from different continents’. So, if the fire doesn’t kill you, the cyanide might just save you! German philosopher Friedrich Nietzsche’s maxim, ‘What doesn’t destroy us makes us stronger’ comes to mind. Hmm, shades of plant and superplant, maybe? Sticking with this rather incendiary topic, using ‘Bayesian Monte-Carlo–Markov-Chain procedures and calibration points from the fossil record’, Tianhua He and colleagues (New Phytologist) concluded that fire may have been a selective force in the origin of Banksia (one of Australia’s most iconic fire-adapted genera) and continued to have an impact on the direction of evolution of that taxon. Okey-dokey, so much for natural – ‘accidental’ – fires, what about ‘deliberate’ ones? Well, a more general role of anthropogenically induced fire in shaping the development of seed traits has been suggested by Susana Gómez-González and colleagues (PNAS). Studying a native annual forb, Helenium aromaticum (Asteraceae), from the Chilean matorral, they showed that fire – which is a novel, anthropogenic disturbance in that ecosystem – is shaping the evolution of seed traits such as pubescence and shape. Now, if we consider humans to be at least a bit intelligent, and they create fire usually with the assistance of tools that have been designed for that purpose, does this not now prove once-and-for-all that intelligent design and/or creation causes what others describe as evolution? Or am I missing the point here?
The January 2011 Annals of Botany is out and I had hoped to put together a press release for one of the papers. Seeds of alpine plants are short lived: implications for long-term conservation by Mondoni et al is one of those papers that states the obvious, but does so in a way that makes you realise that some simple solutions aren’t going to work.
The problem is based around seed banks. These are banks where seeds are stored in cool conditions to prevent them from germinating. The one that grabs a lot of the headlines is the Svalbard Global Seed Vault, but there are others. I can follow that keeping the seeds cool prevents germination and allows storage. Svalbard is naturally very cold anyway, so it seems like a good location for a “Doomsday Seedbank”.* What I hadn’t thought through is that that it’s not just the Arctic that’s cold. The Alps, for example also get cold.
This is what Modoni’s team discuss. Keeping the seeds of Alpine plants isn’t that clever an idea. The seeds are cold anyway. Seeds in warmer conditions need some resistance to the environment they’re in. Modoni et al argue that Alpine plants haven’t adapted for heat, because it’s never been a problem for them. With climate change, this will become an issue very quickly, and it’s likely the plants will not have time to adapt. They’ll driven up to higher and higher slopes as lower altitudes become warmer until they run out of mountain. At this point a seed bank would be a really helpful thing, to store the endangered seeds, but that’s not an option if a cool seed bank isn’t going to prevent germination and decay of seeds.
What I like about this paper is partly the seriousness and difficulty of the problem. These plants are at the base of a food chain for so many animals. If they go, they could take many animal species with them. I think there’s something here with wide appeal and relevance so it should make a perfect story for a press release.
My difficulty is I’ve really struggled to find an accessible start point. It’s a paper about Alpine plants. Which plants? Thistles, plaintains, basically what lowlanders would consider weeds. A story that weeds face extinction is not likely to tug at the heart strings of many readers. The animals that live off them? Insects, gnats, midges. The kind of creature that summer walkers in mountains could happily live without. More animals live off these creatures but the higher up the food chain we go, the further we move from the Botany.
Another way around the problem is to talk about the technique. This is also clever. One way to assess the seeds viability for long-term storage is to store them for a long period of time. That’s great if you have the time and funding to experiment. Modoni’s team took a short-cut. They accelerated the processes by raising the temperature and lightly baking the seeds. I can see why chemically and biologically this works. Heat is the driving force for these processes – so long as it’s not too high. That means more heat is like a fast-forward switch on the experiment. My difficulty is that if I wrote up a press release saying that Alpine plants will germinate in cold temperatures, because experiments with an oven showed they deteriorated at high temperatures, that will simply look insane. It would make sense with an extensive explanation of the method, but the size of a good press-release is one side of A4 and it would be doing well to get 200 words into a paper as a story.
David Frost sensibly suggested seeing if there could be a Sound of Music angle. Alas, Edelweiss was not one of the flowers and we don’t mangle the papers for the sake of making a story. In fact we run the press releases by the authors before putting them out to ensure they’re not horrified by what I’ve written.
So I’ve spent a few frustrating hours with this paper. I can’t shake the feeling there’s some way of writing up a press release that would have worked, but I still can’t see what it was. If you have any ideas feel free to tell me below. It’s too late for this paper, but I might be able to use the comments as inspiration for a future release.
*I’ll skip the problem that if it really is Doomsday, Svalbard will be an amazingly difficult place to access.
Persistence of withered corollas after anthesis (‘corolla marcescence’) is widespread in angiosperms, yet its functional significance does not seem to have been explored. Herrera examines seed production in two southern Spanish insect-pollinated plants, Viola cazorlensis and Lavandula latifolia, and shows that removal of the corollas increases mean number of seeds per fruit in the former, but decreases the proportion of flowers that produce ripened fruit in the latter as a result of higher insect seed predation. Thus marcescent corollas should not be dismissed a priori as biologically irrelevant left-overs from past floral functions.
Seeds in saline environments face a dilemma between allocating reserves to either osmotic balance or growth and development. Zhang et al. show that barley seeds incubated in saline solutions germinate more rapidly than seeds in iso-osmotic PEG solutions. This suggests that barley seeds use salt as a metabolically cheap cellular osmotica, facilitating rapid germination under moderately saline conditions.
Endospermic legumes are abundant in tropical forests and their establishment is closely related to the mobilization of storage polysaccharides and proteins. Tonini et al. adopt a systems approach to evaluate the effects of abscisic acid (ABA), ethylene and sugars on mobilization in Sesbania virgata during the period of establishment. They find that ABA appears to repress enzyme action and retard degradation of storage protein whilst ethylene has the opposite effect. Changes in concentrations of glucose and sucrose during this period suggest that ABA, ethylene and sugars interact to control the process of storage degradation and thus ensure a balanced flow of carbon and nitrogen to the developing seed.