Mycoheterotrophs: the sly swindlers of the plant world

By Helen Roberts

New plant species are discovered all the time. But it is not typical for plants to be discovered in areas that have been meticulously surveyed. Last year, however, a thoroughly unusual species was found on an island in the Kagoshima prefecture, Japan [1].

Gastrodia kuroshimensis is a mycoheterotroph
discovered last year in Japan.
Photo credit:Kenji Suetsugu/Kobe University


Gastrodia kuroshimensis neither photosynthesises nor flowers. Certainly by no means an ornamental showstopper, it is undoubtedly odd looking with fleshy tubers, the absence of leaves and no flowers. In essence, it resembles a pathetic looking fungal protuberance. Strangely enough, it is not a fungus, but a vascular plant. The fact that it does not photosynthesise means it belongs to a peculiar group of plants that are called mycoheterotrophs, which get all or some of their nutrients from a host fungi attached to a vascular plant. The newly found species, Gastrodia kuroshimensis, is what is termed ‘fully’ mycoheterotrophic in that it depends entirely on its association with the fungus throughout its lifecycle. The relationship between it and the host fungi is not mutualistic – it takes all it needs while offering nothing in return. In other words, it’s a big fat cheat.

Mycoheterotrophs parasitise fungi, which are in turn getting their nutrients from a host plant. The fungi that are preyed upon by these cheaters are usually mychorrizal fungi, with mycoheterotrophs often parasitizing a specific arbuscular mycorrhiza (arbuscular mycorrhiza are those that penetrate the cortical cells of plant roots). In this sense, they are dissimilar to parasitic plants like dodder, which obtain their nutrients by directly taking what they need from the vascular tissue using an adapted root.

Who wants flowers?

The second interesting thing about Gastrodia kuroshimensis is that it is entirely cleistogamous, producing flowers that never blossom. Most plants also produce chasmogamous (cross-pollinating) flowers; it is extremely rare to find plants that are entirely cleistogamous. The term cleistogamy means ‘closed marriage’ and the plant produces flowers that are self-fertilised within closed buds. It is essentially a way of ensuring reproduction [2].

The evolutionary reasons are still a puzzle, but it is considered a way of safeguarding fertilisation if suitable pollinators are not around or they have somehow missed the plant or if environmental conditions are not conducive. It can also aid plants in adapting to local habitats, where both sets of maternal genes are passed onto the progeny, thereby removing harmful gene variants. Being cleistogamous also use fewer resources; flowers that are chasmogamous require more energy to produce. However, in most cases chasmogamous flowers are beneficial as they help to provide variability necessary for adaptation, hybrid vigour and negate the effects of deleterious mutations. The reasons for complete cleistogamy remain unresolved but the discovery of Gastrodia kuroshimensis may well help to answer some of these questions.

Other fungi tricksters

Other plants that fall under the mycoheterotrophic category are orchids, monotropes (a subfamily of Ericaceae), members of the Gentian family, certain liverworts and the gametophyte stages of ferns and clubmosses. Some are quite attractive if you like the look of fungal fleshy looking vascular plants with varying hues of red, white and cream. Some are even striped red and white and so commonly known as candystick. Whatever their appearance though, they are unquestionably interesting. But because or their size and rarity they often go unnoticed, lingering in the background like villainous free-loaders.

Mycoheterotrophs at the University of Bristol Botanic Garden

The inflorescences of toothwort in the pollinator display
this week at the Botanic Garden.
Photo credit: Andy Winfield

A wonderful example of a mycoheterotroph at the Botanic Garden is toothwort (Lathraea squamaria L.). It spends most of its time below ground, but in April it sends up aerial inflorescences about 20-25 cm tall. These were in their full glory in the garden a couple of weeks ago, but can still be seen (see photo) in both the pollinator display on the left as you walk in the main gate, or at the east gate.

Unlike Gastrodia kuroshimensis, toothwort flowers are bisexual and pollinated by bumble-bees.

Stop in over the weekend if you get a chance and have a look at this interesting plant.

Helen Roberts is a trained landscape architect with a background in plant sciences. She is a probationary member of the Garden Media Guild and a regular contributor to the University of Bristol Botanic Garden blog.


Sources:

[1] Kobe University. (2016). Plant discovered that neither photosynthesizes nor blooms.
< https://www.sciencedaily.com/releases/2016/10/161014092115.htm>

[2] Allaby, M. (2016). Plant Love: The scandalous truth about the sex life of plants. Filbert Press, pp. 98-103.

Bumblebees who brave the winter

By Nicola Temple

This past weekend, my family and I met with friends in the village of Shipham, in Somerset, for a walk. It was torrential rain, yet we were determined. We dressed ourselves and three children under the age of 10 in waterproofs and set out. We arrived at a local country pub, not more than 3 km away, resembling drowned rats. And as a Canadian living here in the UK, I still marvel at the fact that nobody took one bit of notice at the state of us. It’s what you do. You get wet. You find a pub. You hunker down for a hot Sunday lunch. And you hope it tapers off before you have to head out again. (It didn’t.)

Pollinators, at least of the flying insect variety, aren’t terribly keen on this kind of weather either. Most hunker down for the winter months as there is generally not a lot of nectar to forage this time of year anyway. How they do this depends on the species. Honeybees reduce the colony to a minimal size and rely on their honey stores to see them through, while they dance in order to regulate the temperature of the hive. Most bumblebee colonies die out completely and the queens that mated at the end of the season find a place to hibernate. Solitary bees may hibernate as adults or as larvae, emerging only when the weather conditions are suitable. To each their own.

Martin Cooper spotted this buff-tailed bumblebee queen
foraging on his Mahonia flowers in Ipswich on a sunny
January day in 2015.
Photo credit: Martin Cooper [via Flickr CC]

However, there is one flying pollinator that can be spotted this time of year here in Bristol, and indeed, other warmer regions of the UK. It is the common buff-tailed bumblebee (Bombus terrestris). This species was first spotted during the winter of 1990, in Exeter. Sightings have been increasing ever since and include nest-founding queens, workers and males, suggesting this is a winter generation of the species.

The mated queen will emerge from her subterranean dormant state (diapause) during warm winter weather and set about establishing a new colony. The potential cost of waking up early is that the warm weather could be short-lived and temperatures could plummet. The benefit, of course, is that there’s nobody to compete with for food. If successful, the queen can establish a colony before the other pollinators even wake up from their winter nap.

Introduced plants provide winter forage

Of course, there is potentially another cost to emerging early – there could be nothing to eat. Bees are able to forage at temperatures around 0oC, but if there aren’t enough plants in flower, they won’t find the pollen and nectar needed to sustain the colony. Few native UK species flower in winter, but species introduced by avid gardeners to bring some winter colour to the garden, also bring some much-needed food to the buff-tailed bumblebee.

Researchers at Queen Mary University of London and The London Natural History Society, conducted a study of buff-tailed bumblebees foraging in London parks and gardens during winter about ten years ago. They wanted to see just how much food the bees were finding as food is directly related to the success of the colony.

The researchers found that there was plenty of forage to sustain the colonies and, in fact, the foraging rates they recorded near the end of winter were equivalent to peak foraging rates found in the height of summer. This doesn’t mean that the winter-flowering plants, such as the evergreen shrubs of the Mahonia spp., are providing more pollen and nectar than all the plants in the height of summer. But it does mean that each flower might have more pollen and nectar available because there aren’t other pollinators out and about also using the resource. The bumblebees, therefore, don’t need to go as far to find an equivalent amount of food and so they can collect it at a faster rate.  

Strategies for tolerating cold

Buff-tailed bumblebees aren’t as tolerant to cold as some other bee species; workers will freeze solid at about -7.1oC while queens freeze at -7.4oC. The bumblebees can obviously find warmth in the colony, but they need to forage and therefore be able to tolerate short spells of cold during the winter months. They may even need to tolerate cold temperatures for up to 24 hours as bumblebees often overnight away from the colony when they are unable to return from foraging.

Researchers from the University of Birmingham looked at the different cold tolerances of this bumblebee species a few years ago. They found that 50% of workers died after being exposed to 0oC for 7.2 days while queens could last over 25 days at this temperature – likely due to their fat reserves. However, as the forage study showed, the bees seem capable of finding food sources closer to the colony during winter months, which may reduce the likelihood of them having to endure cold temperatures for a lethal period of time.

These bumblebees may also have adopted some strategies to help reduce their possibilities of freezing. Pollen is an ice-nucleating agent in that it promotes the development of ice at higher temperatures. Other insects have been observed to expel any ice-nucleating agents from their gut when they experience low temperatures to avoid freezing. While this wasn’t observed in the bumblebees, it is a strategy that individuals might employ when caught out in the cold.

The more frequent observation of buff-tailed bumblebees in winter is thought to be a result of warmer autumn temperatures brought about by climate change. In a study from 1969, researchers reported a 6-9 month dormancy of all bumblebees in southern UK, so in a relatively short period of time there has been a considerable change in their seasonal pattern. There seems to be some flexibility in these patterns among bumblebees and for now, establishing winter colonies seems to be working for the buff-tails. However, with so many of our pollinators under threat, there is obviously also concern among the scientific community that more frequent extreme weather events could also spell disaster for these colonies that have selected to brave the winter months. As gardeners, we can perhaps do our bit by planting some winter forage species.

This year, the University of Bristol Botanic Garden will embrace a pollinator theme, with the aim of highlighting some of the lesser-known pollinators that are so important here in the UK. We love our pollinators, but research is still revealing so much about their unique and complex relationships with plants. So watch this space as we share some of these wonderful stories through our blog. We will also be posting pictures of pollinators we see in the Botanic Garden on our Twitter feed and Facebook page. But to see these pollinators in action, take some time to visit the Botanic Garden. Make space in your busy schedule to watch nature at its best – it’s worth it.

Sources:

Alford DV (1969) A study of the hibernation of bumblebees (Hymenoptera: Bombidae) in Southern England. Journal of 
     Animal Ecology 38: 149-170.
Owen EL, Bale JS, Hayward SAL (2013) Can winter-active bumblebees survive the cold? Assessing the cold tolerance of 
     Bombus terrestris audax and the effects of pollen feeding. PLoS ONE 8(11): e80061.          
     doi:10.1371/journal.pone.0080061
Stelzer RJ, Chitka L, Carlton M, Ings TC (2010) Winter active bumblebees (Bombus terrestris) achieve high foraging 
     rates in urban Britain. PLoS ONE 5(3): e9559. doi: 10.1371/journal.pone.0009559 

Keeping your head above water: plants coping with waterlogging

By Helen Roberts

Flooding on the Somerset Levels.
Photo credit: Nigel Mykura [CC BY-SA 2.0],
via Wikimedia Commons

Britain has had its fair share of flooding over the last couple of years. In 2014, the Somerset Levels was under water for weeks and 2015 saw some truly devastating flooding occurring in the northwest of England. Flooding can have detrimental effects on our own lives, but also on plant communities.

Waterlogging of plants can cause chlorosis (loss of the normal green colour) of the leaves, root rot and eventually death. It’s a common problem that many gardeners face every day and there are different techniques to cope with this ever persistent problem on our shores. Precautions are even taken at the University of Bristol Botanic Garden during this wet weather.

“As far as the garden borders go, we’re very careful about never walking on them when there’s been heavy rain,” explained Andy Winfield, horticultural technician at the Botanic Garden. “If we have to get on a border for any reason, we use a board and then fork over where it was to prevent compaction and a pan forming. When a pan forms, then water is more likely to sit on the surface and create problems.”

How does waterlogging affect soils and plants?

The profile of a soil will greatly affect its interaction with water. Soils are composed of solid material with spaces filled with water, gases, roots and other living organisms – these attributes impact water retention and drainage. For example, clay soils have small pore spaces and so retain more water compared with sandy loams.

Subsoils can also influence soil structure and its interaction with water. Waterlogged soils are not only affected by the amount of water coming into the system, but by the soil’s ability to disperse and absorb that water.

When soils are waterlogged, the air spaces between the particles are filled with water and the movement of gases within the soils is inhibited preventing the roots from respiring properly. Gases such as ethylene and carbon dioxide begin to accumulate, which leads to further negative impacts on root growth. Anaerobic processes begin to changes the soil biochemistry, which leads to plant death through the build up of toxins within soils.

What is happening to plants at a cellular level when faced with anoxic or hypoxic conditions? 

When plants are waterlogged, they are not getting enough oxygen via the roots for cellular respiration and energy production. Because the plants cannot obtain oxygen via the roots, plants turn on their own energy reserves. This is much like when we use our muscles during strenuous exercise and we can’t get sufficient oxygen to the hard working cells – the cells undergo anaerobic respiration, which produces lactic acid. Plants can also undergo anaerobic respiration, but it is not sustainable and eventually, the plant dies as the demand for energy exceeds the supply.

Until recently little was known about how some plants cope with the stress of waterlogging. However, researchers from the Max Planck Institute of Molecular Plant Physiology, with colleagues from Italy and the Netherlands, have discovered a protein that triggers the activation of stress response genes when oxygen levels drop due to waterlogging. This protein is attached to the cell membrane under normal aerobic conditions, but when levels drop it detaches from the membrane and relocates to the nucleus where it switches on the stress genes. When oxygen levels return to normal, the protein degrades and the stress response genes switch off again.

How some plants have evolved to cope with anoxic and hypoxic conditions

When out walking as a child on Exmoor, I would often pick the stems of the soft rush, Juncus effusus, and peel back the green outer coating to reveal the soft, husky white pith inside. I was amazed when an adult told me this material was once used for making rush lights. The pith would be extracted from the rush leaves and combined with fat or grease to provide a source of artificial light. This pithy material is interesting though in this context as it contains a tissue called aerenchyma, which is usually found in the roots and stems of many hydrophytes (plants adapted for living in water). The tissue has large interconnected intercellular gas spaces that help to oxygenate the roots and increase buoyancy.

Other plants adapted to soggy conditions will produce fine surface roots called adventitious roots. These roots scavenge oxygen from the surface where there is a thin aerobic layer. Many of the Melaleuca species, mostly from Australia, use this way of coping with water hypoxia.

Some plants are adapted to rise above it all; they elongate their shoots to get above the water, as is the case with some floodplain Rumex species (docks and sorrels). Nymphaea species (the water lilies) – which you can see in the Botanic Garden glasshouses –  have a hugely elongated petiole, often more that two metres long, to keep their leaves and flowers at the water surface.

Arial roots (pneumatophores) of the grey mangrove
(Avicennia marina var resinifera) from South Australia.
Photo Credit: Peripitus (Own work) [GFDL, CC-BY-SA-3.0 )
or CC BY-SA 2.5-2.0-1.0 ], via Wikimedia Commons

Large tree species have also adapted their roots to cope with swamp-like conditions. These strange looking roots are known as pneumatophores – woody extensions that grow vertically upwards from the underground root system to reach above water and capture that much needed oxygen. The bald cypress, Taxodium distichum, which is found in the southern USA in lowland river floodplains and swamps, forms these roots that look like knees sticking up out of the water. The actual surface of the root is pockmarked with many lenticels, which are small stomata-like pores found in the bark that allow gaseous exchange. Other swamp and mangrove species have variations of these root adaptations to cope with low oxygen levels including pencil and cone roots (which belong to the pneumatophore group) and other types of aerial roots like knee, stilt, peg and plank roots. These roots differ in both their morphology and function, but are ultimately adapted to cope with waterlogging and often saline conditions.

The importance of wetlands as carbon sinks

Waterlogged lands are not all doom and gloom, in fact, bogginess is vitally important in terms of the Earth’s climate. Peatlands fall into that category. They act as important carbon sinks and currently cover about four per cent of the Earth’s land surface. Drainage of these areas of peatlands and wetlands for agricultural use leads to increases in greenhouse gas emissions. Researchers are actively trying to understand the effects of climate change on peatlands globally and there have been pushes to effectively  conserve and manage these precious ecosystems.

Sources:

Guillermina M. Mendiondo, Daniel J. Gibbs, Miriam Szurman-Zubrzycka, Arnd Korn, Julietta Marquez, Iwona Szarejko, Miroslaw Maluszynski, John King, Barry Axcell, Katherine Smart, Francoise Corbineau, Michael J. Holdsworth. Enhanced waterlogging tolerance in barley by manipulation of expression of the N-end rule pathway E3 ligasePROTEOLYSIS6. Plant Biotechnology Journal, 2015; DOI: 10.1111/pbi.12334

Francesco Licausi, Monika Kosmacz, Daan A. Weits, Beatrice Giuntoli, Federico M. Giorgi, Laurentius A. C. J. Voesenek, Pierdomenico Perata, Joost T. van Dongen. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature, 2011; DOI: 10.1038/nature10536

Daniel J. Gibbs, Seung Cho Lee, Nurulhikma Md Isa, Silvia Gramuglia, Takeshi Fukao, George W. Bassel, Cristina Sousa Correia, Françoise Corbineau, Frederica L. Theodoulou, Julia Bailey-Serres, Michael J. Holdsworth. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 2011; DOI: 10.1038/nature10534

Some like it hot

By Helen Roberts

With the dismal wet wintry weather prevailing in the UK at this time of year, most people look forward to the return of warm long days, evenings outside and picnics on the beach. Things can look a little dreary and dull in people’s gardens at the moment, before the arrival of spring and its profusion of bulbs and other spring flowers. The Mediterranean collection at the University of Bristol Botanic Gardens helps to remind me of summer sun and balmy places.

Maquis: scrubland vegetation of the Mediterranean

Maquis shrubland in Conca de Dalt of Catalonia, northeastern Spain.
Photo by Gustau Erill i Pinyot.
Licensed under CC BY-SA 3.0 via Wikimedia Commons 
The Mediterranean Basin of Europe and North Africa display shows examples from different vegetation biomes; the collection includes evergreen forest, maquis or macchie and garique. Many of the highly aromatic and fragrant plants are associated with maquis vegetation. The maquis biome, which often includes leathery broadleaves, evergreen shrubs and small trees, usually occurs on the lower slopes of mountains bordering the Mediterranean Sea.
The climate of the maquis biome is characterised by long dry summers and short mild wet winters, with low annual rainfall. Ocean currents and fog influence the temperature and limit the growing season. The plants that grow here cope with the very hot summers by entering a slow growth period or dormant phase so they can resist long periods of drought.
Plant defences in this harsh environment are numerous. Many shrubs and low growing vegetation have thick tough leathery leaves, which reduce water loss but also deter hungry herbivores from grazing. Many plants contain volatile organic compounds (VOCs). These chemicals help facilitate interactions between plants and the environment – from attracting pollinators and seed dispensers to warding off pathogens, parasites and herbivores. When a plant is under attack from a herbivore, for example, it will release a chemical cocktail of VOCs, some of which have been found to attract natural predators of the herbivores. VOCs are also good at leaching into surrounding soil and so will deter the growth of other plants.
Plants containing VOCs are often very flammable, which is partly why areas of maquis are prone to wild fires.

Pyrophytes need a little fire in their lifecycle

Montpelier cistus (Cistus monspeliensis).
Photo by Jean-Pol GRANDMONT
via Wikimedia Commons
Many of the plants in the maquis biomes are pyrophytes (fire loving plants) and require wild fires for reproduction, recycling of nutrients and removal of dead vegetation. Pyrophytes can be classed as active or passive. Active pyrophytes actually encourage fires as they often require fire in order to reproduce. Passive pyrophytes resist the effects of fires.
An active pyrophyte growing in the University of Bristol Botanic Garden maquis biome is Cistus monspeliensis, commonly known as the Montpelier cistus or rock rose. When a fire starts, Cistushas evolved to burn. This combustible conclusion to the adult plant helps destroy competing plants near to it. However, unlike its competitors, the fire will mechanically rupture the seeds of Cistus and the smoke and heat will trigger germination of the next generation. The Cistus seedlings have the advantage of beginning life in a competitor-free environment.
A closed cone and foliage of Pinus pinea.
 Licensed under CC BY-SA 2.5 es via Wikimedia Commons 
Pinus pinea (the stone pine) is also in the Botanic Garden’s collection and it is a passive pyrophyte. It has a thick bark with high moisture content to help it resist fire. Its hard-coated fire resistant cones open when exposed to high temperatures. This is particularly useful in the harvest of the desirable seeds, known to many of us as pine nuts. As the tree grows, it self-prunes the lower branches, which helps prevent the fire travelling at ground level from jumping up into the canopy and potentially destroying the tree.
Some species spring back from fire events by sprouting new growth from the old. There are two such sprouter species in the Botanic Garden’s collection. The carob tree (Ceratonia siliqua) re-sprouts from epicormicbuds that lie dormant beneath the bark. These buds are normally suppressed by hormones produced by active shoots, but after a fire event and the destruction of the foliage, the buds are activated. Erica arborea (tree heath) re-sprouts from root crowns so is known as a below ground sprouter. It produces seed in the first post-fire summer.
Fire adapted plants of the maquis biome are only a handful of those plants making up the Garden’s Mediterranean collection. The collection also includes plants (some of which are also pyrophytes) from the southwestern tip of South Africa and displays are also under development from the Western andSouthern Australian, Chilean and Californian Mediterranean climate regions.
The half hardy plants of the Mediterranean collection are planted out in each respective biome in the summer, whilst more tender plants are protected from our cooler Bristol temperatures in the warm temperate and cool zones of the glasshouses. The outdoor collection sits on a south facing rocky bank to maximise the amount of sun and aid drainage. The path meanders through the collection allowing visitors to appreciate the appearance and fragrances of the different plants. These are all good things to look forward to in the summer months, but meanwhile if you have the chance to warm yourself in front of a crackling fire, think of those volatile fire-loving plants!