Article contributed by CVN member Véronique McIntyre.
While the Botany/Mycology Group was at Kitty Coleman Park, leader Jocie B. found a hemlock branch infested with dwarf mistletoe (Arceuthobium tsugense).
(Photo: Véronique McIntyre)
A close-up of the branch shows the reason for the “dwarf” qualifier. It also demonstrates the different shades of green between mistletoe and western hemlock needles, which point toward different photosynthesizing abilities.
Under the guise of taking pictures, I stayed a bit behind the group and witnessed the following conversation between the mistletoe and its host.
“Parasite! They called me a parasite!”
“And what exactly do you think you are? A benevolent association? You’re stealing my food and slowly starving me just so you can live.”
“Do you think I have any choice? I am stuck at the top of a tree – well, not anymore, since you broke from the main trunk and fell to the forest floor – which makes me an epiphyte like all mistletoes the world over. So, how am I supposed to get the water and minerals I need for photosynthesis?”
“Other epiphytes manage without being parasites; they form cups that collect and keep rainwater. Or, they live in tropical countries where water is plentiful. Or, like licorice fern (Polypodium glycyrrhiza), they grow along the trunks of bigleaf maple trees (Acer macrophyllum), spreading their roots under the mosses which keep the trunk moist. You choose to steal. That makes you a parasite. By the way, how did you end up at the top of my tree?”
“That wasn’t easy. A huge stroke of luck, I would say. Like the other twenty-six species of dwarf mistletoe in the world, my species can only grow on conifers (Cupressaceae and Pinaceae). For us it is mostly on western hemlock (Tsuga heterophylla), sometimes on shore pine, grand fir or Engelman’s spruce. We make it easy for botanists: if you find dwarf mistletoe on a branch of Douglas fir, it is most likely Arceuthobium douglassi. On a branch of shore pine (Pinus contorta), it is probably Arceuthobium americanum.[1]
We are Arceuthobium tsugense by the way. I think, anyway. I know, I have a complicated name, Arceuthobium means “lives on juniper” in Greek, from the species that lives in Europe, Asia, and Northern Africa on — would you guess it? – juniper. We go by the nickname “mistletoe”, apparently from the Saxon “mistl-tan” meaning ”different twig”, which describes us quite well as we grow on our host. Even though it is highly unlikely any Saxon ever set an eye on us. Or “mistel” (= dung) and “tan” (= twig) because our European cousins are spread by the seeds transported by birds’ feces. But, back to your question. My first stroke of luck came when my seed landed on the right tree.”
“Luck for you, not for me.”
“I know, I know, you are such a spoilsport. My seed landing on a tree belonging to the right species has been made easier for the last century or so by the practice of replacing trees that were cut down with trees mostly from the same species, planted close to each other. Much less distance between hemlocks… loss of diversity for some, gain for us. Now, a seed landing on a tree usually simply falls to the ground where it germinates. Not our seeds. We belong to the global family Santalaceae (sandalwoods), along with other root, stem, and aerial parasites. Like them, all our fruits contain one seed each. This seed is surrounded by a sticky mucilaginous tissue called viscin, made of cellulose microfibrils embedded in a matrix of hemicellulose and a bit of pectin that is sensitive to humidity. It looks like only Santalaceae have the genes needed to produce viscin, by the way. A beautiful adaptation to parasitism that humans highjacked to produce birdlime.“
“And you are proud of it? Really?”
“I am. It took between 38 and 46 million years to perfect aerial parasitism in my family.[2] [3] The common ancestor to Arceuthobium and Visca (Christmas mistletoe for instance) split 42 million years ago according to our DNA sequences,[2] and you can find fossils of at least 6 species of Arceuthobium in Baltic amber more than 25 million years old.[3] Imagine my family tree!”
“I can picture all my ancestors falling victims to your malevolence.”
“Me, me, me, that’s all you can see. Look at the whole picture! So far, remains of direct evidence for parasitism are not preserved in the amber specimens. However, the small size and reduced morphology of my ancestors fossilized in amber can be interpreted as adaptions to a parasitic lifestyle. Anyway, our ancestors were parasites on roots. It takes a lot of mutations to go from there to parasitizing branches.
But let’s go back to the viscin. If the air is humid enough, this matrix forms sticky fibers.[4] When the seed is mature, the fruit explodes, which is quite a feat in itself, as it needs the exact balance of temperature and humidity to occur, and so at the end of last September I was shot five to fifteen meters away from my mom.[5] Most likely five, as there are enough trees here to have intercepted me. I never knew my dad as he was living on another mistletoe (we are a dioecious species, meaning that our females and males form on different plants). Pollen in our family is spread by wind and by insects and can travel up to 150 meters.[4] When mature, the female flower exudes a pollination droplet that intercepts the pollen, like you would expect in gymnosperms, not in angiosperms![6] I heard some neighbours tell stories of being transported around here by sticking to the toes of birds or the fur of small mammals. Maybe they were just boasting.”
“OK, fine, but how did you stay at the top of my tree then? Why did you not fall to the ground, where you would have died since you need a live tree to live, confirming you are a parasite?”
“You really won’t let go of that will you? My seed had the good sense to land on the needle of a twig that was less than five years old. In other words, you. Older twigs are not suitable, probably because the bark is too thick. Consider yourself lucky: the mistletoe on shore pine can infect branches up to 60 years old. I wish I could do that, but I found you. And that has worked out just fine.[7]”
“I was just a wee baby then!”
“And quite the crybaby, too. Once my seed was on the needle, the viscin made it solidly stick to it until the first fall rain made it slide down. Viscin works a bit like mucus: slippery when wet and solid when dry. Note that the whole time I was stuck on that needle I could have been eaten or infected. That would have been a shame. The odds of our seeds surviving to adulthood are infinitesimally small.”
“I wish your predators and pathogens were more efficient. Or that the rains in the fall wouldn’t come before December.”
“Blah, blah, blah. Now where was I? Oh yeah, again, I was at great risk of being washed away to the ground, but as luck had it, I nicely slid to the bottom of the needle and got wedged there, where I waited for the spring. So many of my sisters and brothers slid to the ground though. My seed germinated once the days lengthened, and the elongating radicle grew along your surface until it met a break in the bark at the base of the needle.”
“Wait a minute, how could you grow? You were not pumping my sugars yet, since you were still outside of me.”
“Correct. Luckily for me, my seed contains reserves, called endosperm, and ours, contrary to other plants’ endosperms, can perform photosynthesis. What a gift those parasitism adaptations are! But of course, if I hadn’t been able to find a break in your bark quickly enough, my reserves would have died out, and me with them.[7]”
“So, you are insinuating that I helped you get inside my tree?”
“You did, like it or not. I did not trigger that first break. And I picked up from you some chemical molecular signals that confirmed to me you belonged to a good species to infect. So, I would say you were almost a willing participant in our relationship. A brother even, as some human dictator says to justify his invasions, so why shouldn’t I? The tip of my radicle, aided by my producing lots of germination stimulants, then formed a holdfast by quickly dividing my cells. From there a peg (called a haustorium by people who want to sound clever, from the Latin word haustor, meaning drinker or drawer of water) penetrated your bark tissue, crushing it as well as whatever was beneath it. I also produced some enzymes to degrade your cell walls.
I was very young then and I don’t remember if I also perceived haustoria inducing factors (HIFs) secreted by you, although I know many parasites do.[8] Judging by the timeline in other species, four to eight days after infection I had established a xylem bridge with you and was getting your water.[8] I then established a connection to your phloem, thus gaining access to your sugars.
You should know that along with your nutrients, I also absorb your defensive chemical compounds and use them for my own defence, for instance against Caliciopsis arceuthobi and Colletotrichum gloeosporiodes, two of our major fungal parasites.[7] Some humans have even tried infecting us with them. Imagine! I stayed for two long years under your bark in total darkness as I was developing a network of strands that reached your phloem and your cambium, and thickened that modified root that attaches me to you. You see how photosynthesis would not have been possible anyway; [7][8] I needed your sugars, minerals and nitrogen to survive in the darkness for so long.“
“Jeez, how come I was not able to prevent you from doing all that damage?”
“Humans found that microRNAs were transported from the parasite Cuscuta campestris to its Arabidopsis thaliana host, and these miRNAs could effectively silence the expression of host genes important for resistance to the parasite.[7] Maybe that’s what I did, but I can’t remember.”
“I guess 40 million years is long enough to come up with very sneaky and dishonest ways to harm others.”
“Maybe. Anyway, seen from the outside it took you two years to look a bit puffy, swollen maybe even, but besides that nothing showed. Once my little strands were in your phloem I was almost out of the woods—suddenly, I had access to all your caches! Those vessels go from your needles and transport the products of your photosynthesis to where they are needed. Sugars galore! Luckily, my genes for production of cytokinins and other hormones went into overdrive, which increased the transfer of sugar from you to me. And they continue to do so. That gave me the energy to produce my external shoots you see on your branch, with my beautiful, segmented stems that bear scalelike simple opposite leaves, while at the same time developing extensively inside you. And two years later I was able to produce flowers, thanks to your sugars. Now you really started to swell as I pushed my shoots out of your bark in concentric zones of increasing diameter year after year.”
“Hey, your shoots are green. Why would you need my sugars when you have chlorophyll and chloroplasts, can photosynthesize, and now are outside of me, meaning under the sun?[9]”
“It’s not enough to have both chlorophyll a and b like all plants, you need the right amount, and I only have 1/5 to 1/10 of what you have in your needles.[6] I guess that’s why my leaves are so small. Plus, you are lucky: you can fix many times more carbon using photosynthesis than you expel in the air via respiration. Therefore, you have an excess of carbon in the form of sugar, which you can devote to your growth, your reproduction, fighting diseases, etc. Me, I am not so lucky. Mother Nature only granted me a system that allows me to fix the ridiculous amount of 25 to 30% of the carbon I expel. There is no way I can stock the sugars, amino acids, minerals and other substances I need, in the amounts I need. Far from it. I do not know if it is the chlorophyll that is wanting, or the regulation of its production, but the fact is I can’t live on my own and need an extra source of sugar. I need a host.[10]”
“And it had to be me.”
“Well, you were available. My shoots also help in the transfer of sugar from you to me since they transpire quite a lot. You see, I don’t have any phloem I could connect to yours. Therefore, the nutrients I need arrive with water as a flow from you to me and never go the other way. My shoots are generally short-lived and leave “basal cups” when I shed them. You can see one of them in Figure 2. Maybe that’s because they work too much extracting those nutrients, or, since they are quite flammable, it is a protection. I don’t want to end up in an inferno.”
“So, on top of everything else, you are a fire hazard.[11]”
“That’s part of my charm, yes, I can be very hot. But no, in fact you are responsible—you drop your branches around because you find my tiny little shoots too heavy, and they are combustible. And don’t go telling me that I weaken big branches enough that like you, tiny twig, they break and might fall on unsuspecting people in parks creating some hilarious situations. You are the one who dropped to the ground, not me.”
“A pleasure to be around you.”
“I don’t need your sarcasm. In fact, I am quite helpful. You see, if you had not clumsily fallen from your tree, I would have changed your hormone balance and induced the formation of beautiful exuberant abnormal growth of branches that are called witches’ brooms. When they are large, the branches break off from the extra weight, which changes the canopy and the amount of light that reaches the soil and allows trees like Garry oaks (Quercus garryana) to prosper and form seeds.
Also, lots of animals, squirrels for instance, are known to selectively feed on the swollen nutritious tissues formed by my infections, especially in winter when there are not many other resources available, and humans have picked the mushrooms that squirrels would normally eat. Up to 85% of their diet is mushrooms, did you know that? Well, I provide extra energy to them at no cost to me. Imagine, instead of falling to the ground, being slowly gnawed on by a red-bellied squirrel…. Others use the witches’ brooms as nesting sites: birds such as Northern Spotted Owls and Marbled Murrelets, and small mammals such as red squirrels, the American marten, and woodrats.[11] And many arthropods such as mites and spiders use them as a foraging site, to be in turn eaten by birds. Some are even specific to mistletoes such as larvae of the moth Filatima natalis, but also bugs (Neoborella tumida) and several species of Coleoptera and Thysanoptera.[5][12] So, you see, thanks to me, the species diversity in the forest is increased. This is well worth a few of your kind dying and falling off.“
“When you landed on me, I should have realized I was doomed.”
“And what would you have done about it? Severed yourself from your tree? You did that, but too late. See, some of my strands managed to reach your cambium, and as you produced more wood every year, they got embedded into it. By now a good 20 to 30 cm of what’s left of your twig on your tree is infected, not just the little part you detached. Once we have infected a tree, we are impossible to extract. I think your tree is lucky. If my seed had landed closer to one of your major branches, by now your trunk would be infected, with large knots and spongy wood, jeopardizing your growth by up to one half, draining from you enough sugars to impede the production of your seeds, most likely distorting your shape, and leaving you more susceptible to diseases and insect infestations. This would have shortened your life and cost you your top.[13][14] So, you should thank me for having only taken a wee little amount of your precious reserves of sugar.”
”You are quite the manipulator, you know that? I know for a fact that dwarf mistletoes are at their worst in western North America in terms of damages inflicted to conifers: they manage to kill up to ten percent of trees in Oregon.[5]”
“Well, maybe it’s because one little dwarf plant on a tree doesn’t do much damage, but when suitable trees are too close to each other, an infected tree can repeatedly infect its neighbours. Don’t forget that some seeds slide down from the needle they landed on, but they don’t reach the ground, they simply infect a lower branch. A single Tsuga heterophylla infected by us can produce 73,000 mistletoe seeds a year.[4] Maybe my pumping of your water and sugars also triggers water stress and strongly reduces carbon assimilation under stressful conditions. Global warming might be one of those conditions. You can hardly blame me for that one, though! And anyway, a dead tree is a haven for all sorts of birds and mammals looking for cavities as shelters or to nest. Not to mention the many insects that feed on it, lichen and mosses that develop, and more.”
“It’s clearly too late for me now, but one thing I am wondering is how you managed to infect me. I mean, I am a completely different organism than you. Humans can graft plants, but it works only between plants that are close phylogenetically. I am not saying we have self-recognition cells like some white blood cells in mammals, but we must have a unique ability to overcome tissue incompatibilities and self/non-self recognition.[8]”
“Well, I really have no clue about that. I can only take the credit for having managed to do it.”
“Still, I might grow over fifty metres high, and you are a mere seven centimetres long. You inflict quite a large amount of damage for something so small.”
“Lots of parasites do that. The sleeping sickness agent for humans can only be seen using a strong microscope. Look at it this way: I am a natural thinning agent, just like bark beetles or wildfires. In the long term, I increase species diversity of forest. Not a small feat for a wee little species like me that is not in abundance!“
“So, there is nothing, nothing at all that can get rid of you then.”
“I would not say that. People could space the trees they plant much more, and plant more varied species that we cannot infect. As I said, our seeds don’t go farther than 15 metres. A few more horrible methods have been tried, involving herbicides that are injected into infected limbs below the point of infection, accumulate in us, and eventually kill us without severely affecting our host. But you know how chemicals have a nasty way of looking inconspicuous, and then, sometimes years later, major damages are discovered. Unless you are raising trees to cut them down—and who would be that cruel and greedy—consider that we are only slowly encroaching on the surrounding forest, less than one metre a year usually.
So, maybe the best is to let us live? That’s what we have done for the last 40 million years, and yet forests are still around. Within a few more million years you guys might develop some defences against us that would be more efficient, like European trees did against their local mistletoe. Or not. Like everything in nature, we have our advantages and benefits. Live and let live is my motto.”
“Right, what a liar. I am dying thanks to you.”
“Great, we agree to disagree then. I am all for teamwork with you to increase diversity. And we are dying together anyway, since I need a live tree to live on.”
References
- List of Arceuthobium species. Wikipedia.
- Romina Vidal-Russell and Daniel L. Nickrent. 2008. The first mistletoes: Origins of aerial parasitism in Santalales. Molecular Phylogenetics and Evolution 47: 523–537. PDF.
- Eva-Maria Sadowski, Leyla J. Seyfullah, Carol A. Wilson, Clyde L. Calvin and Alexander R. Schmidt. 2017. Diverse early dwarf mistletoes (Arceuthobium), ecological keystones of the Eocene Baltic amber biota. American Journal of Botany 104(5): 694–718.
This resource includes stunning pictures of amber-embedded samples of very old dwarf mistletoes.
- Nils Horbelt, Peter Fratzl, Matthew J Harrington. 2022. Mistletoe viscin: a hygro- and mechano-responsive cellulose-based adhesive for diverse material applications. PNAS Nexus 1(1) pgac026.
- F. G. Hawksworth, D. Wiens and B. W. Geils. 2002. Arceuthobium in North America. Mistletoes in North America. USDA Forest Service Gen. Tech. Rep. RMRS-GTR-98, Chapter 4. PDF.
- Southern Illinois University. 2010. Life Cycle of Arceuthobium (dwarf mistletoe).
- Sue Ellen Askew. 2007. Assessment of Colletotrichum gloeosporioides as a biological control of hemlock dwarf mistletoe (Arceuthobium tsugense). UBC Theses and Dissertations.
- Anna Kokla and Charles W. Melnick. 2018. Developing a thief: Haustoria formation in parasitic plants. Developmental Biology 442(1): 53–59.
In particular, see Fig. 1, a very clear diagram of haustoria formation that is probably similar to that of Arceuthobium.
- J. Roger Miller and R. D. Tocher. 1975. Photosynthesis and respiration of Arceuthobium tsugense (Loranthaceae). American Journal of Botany 62(7): 765–769.
- James Roger Miller. 1973. Photosynthesis and respiration of Arceuthobium tsugense. Dissertations and Theses, Paper 1689. PDF.
- James T. Hoffman. 2010. Management Guide for Dwarf Mistletoe Arceuthobium spp. US Forest Service. PDF.
- D.C. Shaw, D.M. Watson and R.L. Mathiasen. 2004. Comparison of dwarf mistletoes (Arceuthobium spp., Viscaceae) in the western United States with mistletoes (Amyema spp., Loranthaceae) in Australia—ecological analogs and reciprocal models for ecosystem management. Australian Journal of Botany 52(4): 481-498.
- George N. Agrios. 2005. Plant diseases caused by parasitic higher plants, invasive climbing plants, and parasitic green algae. Chap. 13 in Plant Pathology. 5th ed. Academic Press.
- Stephen J. Calkins, David C. Shaw and Yung-Hsiang Lan. 2020. Transformation of western hemlock (Tsuga heterophylla) tree crowns by dwarf mistletoe (Arceuthobium tsugense, Viscaceae). Forest Pathology 51(1). PDF.
