The Color of Light

Sunshine, to our human eyes the light appears white, but buried within are all the colors of the rainbow. In order for you or I to detect the colors that compose white light we need help. Shining light through a prism is one way I know to separate light into its many colorful components. Plants, on the other hand, need no such help. They have proteins called photoreceptors that enable them to detect different wavelengths of light. There are several different types of photoreceptors. Phototropins sense blue light, phytochromes sense red light, and neochrome is a chimeric protein that has the ability to sense both blue and red light. 

Light, especially the blue and red portions, are the main types plants use to run their photosynthesis machinery. When taller plants shade out shorter plants they alter both the quantity and quality of the light that reaches the plants below. Thus it is important that plants can detect the light quality in order to respond appropriately, by either growing away from shady spots or altering how they develop. 

A few ferns hanging out with their mossy pals.

A recent study was published that literally sheds some light on the evolution of these light sensing photoreceptors. Neochromes, the light sensing proteins with dual abilities, are present in only two groups of plants, the green algae and the ferns. Previously, scientists thought that these two groups independently evolved neochromes. But this new research proposes a different explanation. They found that the hornworts, a small group of bryophytes, also have neochromes and their proteins are closely related to those in ferns. They are so similar in fact that they were most likely transferred from hornworts to ferns. 

Horizontal gene transfer is a pretty wild thing that can happen in biology. One organism, potentially distantly related to another, can transfer some of its genetic code to another organism. If it is helpful the organism will keep the new piece of DNA, use it, and pass it on to its offspring. Scientists think that neochromes were very useful for ferns. Growing in the shadows of taller flowering plants, neochromes enabled ferns to take full advantage of low light conditions, thrive, and diversify. I think the ferns should send a thank you note to the hornworts for that super useful gift. The transfer of neochromes from one to the other happened over 150 million years ago, but you know what they say, better late than never.

Fay-Wei Li, Juan Carlos Villarreal, Steven Kelly, Carl J. Rothfels, Michael Melkonian, Eftychios Frangedakis, Markus Ruhsam, Erin M. Sigel, Joshua P. Der, Jarmila Pittermann, Dylan O. Burge, Lisa Pokorny, Anders Larsson, Tao Chen, Stina Weststrand, Philip Thomas, Eric Carpenter, Yong Zhang, Zhijian Tian, Li Chen, Zhixiang Yan, Ying Zhu, Xiao Sun, Jun Wang, Dennis W. Stevenson, Barbara J. Crandall-Stotler, A. Jonathan Shaw, Michael K. Deyholos, Douglas E. Soltis, Sean W. Graham, Michael D. Windham, Jane A. Langdale, Gane Ka-Shu Wong, Sarah Mathews, and Kathleen M. Pryer. Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. PNAS, published ahead of print April 14, 2014, doi:10.1073/pnas.1319929111

Additional coverage of this research can be found at these links: National Geographic, ScienceDaily, and The Economist. 

For more on plant colors, check out Johnna's April edition of the Berry Go Round plant carnival. My favorite is the post about the iridescent fruits of Pollia condensate. Pretty cool that they are the shiniest living things on Earth!

The Signature of All Things: Part 2 - Catching bryophyte fever

***Spoiler Alert***

This post may contain plot details and quotes from Parts 1 & 2 of The Signature of All Things. Proceed with caution!

The second part of The Signature of All Things focuses on the childhood of the main character Alma Whittaker. In my mind the true main characters, the bryophytes, have yet to truly arrive on the scene. There is a brief mention of mosses being used by birds as material for nest building. Alma also uses mosses to fill the chinks in the walls of her study to cut down on winter drafts. Hornworts come up during a scientific discussion between Alma and her colleague George Hawkes. He describes them to another friend as "...among our least sophisticated plants-". I take mild offense to that statement. I think hornworts are super interesting and highly sophisticated in their ability to establish a mutualistic interaction with cyanobacteria (blue-green algae). They have pores on the underside of the plant that open to allow the algae to enter. The algae then live and grow inside of the hornwort helping to fix nitrogen, making it available for the hornwort to use. I think that establishing a relationship like that is pretty sophisticated. Don't you?

At the tail end of Part 2 bryophytes take their rightful place at center stage. Alma has a revelation that right beneath her nose, on the land she has known her entire life, is a world unexplored. The miniature world of mosses. An entire rock may be covered by dozens of species that occupy distinct niches. A little sunnier over here, a little wetter over there, makes for diverse habitats even within a few feet. It is amazing how small changes in the microclimate can make such a big difference to the bryophytes. The description of Alma's epiphany to focus her botanical energies on mosses is full of lovely imagery, such as the passage below. 

"Now the miniature forest below her gaze sprang into majestic detail. She felt her breath catch. This was a stupefying kingdom. This was the Amazon jungle as seen from the back of a harpy eagle. She rode her eye above the surprising landscape, following its paths in every direction. Here were rich, abundant valleys filled with tiny trees of braided mermaid hair and minuscule, tangled vines. Here were barely visible tributaries running through that jungle..."

Having done so myself, falling in love with bryophytes is an amazing experience. Upon closer inspection, you realize that there is a world of wonder to explore in miniature. The closer you look the more there is to discover. An adventure that can last a lifetime. 

Photosynthesis in Hornworts

Photosynthesis is the most important biological reaction on the planet. It creates the sugars and starches that we and other animals rely upon for food. Photosynthesis also helps to regulate the climate by binding up carbon from the air to keep the planet cooler. Plants need carbon dioxide, water, and light to carry out photosynthesis. 

Hornworts have a cool structure called a pyrenoid that helps to increase the rate of photosynthesis in these plants. Pyrenoids increase the concentration of carbon dioxide close to the enzyme RuBisCO, which is critical for photosynthesis. A recent study examined pyrenoid evolution in the hornworts, the bryophyte lineage most closely related to flowering plants. They asked whether the evolution of the pyrenoid in hornworts was correlated with historically low levels of carbon dioxide in the atmosphere. It is predicted that low levels of carbon dioxide in the atmosphere would put pressure on plants to evolve mechanisms that enable them to increase the concentration of carbon dioxide in their cells in order to increase rates of photosynthesis. 



Villarreal, J. & Renner, S. (2012). Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years Proceedings of the National Academy of Sciences, 109 (46), 18873-18878 DOI: 10.1073/pnas.1213498109

Their results support the pyrenoid structure evolving 5 or 6 times across the hornworts (transition from blue to red in the figure below). Pyrenoid evolution does not appear to be synchronous, each time the pyrenoid evolved across the tree was at a different time in the past. If they had evolved in response to changes in the atmosphere, we would predict that they evolved at the same time. They also did not find a relationship between low atmospheric levels of carbon dioxide and pyrenoid evolution. Even when atmospheric carbon dioxide levels were low, new hornwort species evolved that did not have a pyrenoid. If the pyrenoid was really advantageous, we would predict that when the carbon dioxide levels were low only species with a pyrenoid would evolve new species. Based on this and other findings, they propose that the evolution of the pyrenoid may be related to something other than the atmospheric concentration of carbon dioxide

Figure 1 from Villarreal & Renner 2012. This shows the relationships
between different species of hornworts. The species in blue do not have pyrenoids
and the species in red do have pyrenoids. The black and white inset images show the
different types of pyrenoids found in hornwort species. 

Relationships between the Three Groups of Bryophytes

I got an email this week from a colleague about the state of the relationships among the three groups of bryophytes: Mosses,  Liverworts, and Hornworts.

The first questions to consider - Are they three separate lineages? OR One monophyletic lineage?

If they are three separate lineages, what order should they be placed in relative to tracheophytes (plants that have tracheids, a special type of xylem)?

Well it all depends on which data are used.

Data from sperm ultrastructure (Garbary et al. 1993) and DNA data from entire chloroplast genomes (Nishiyama et al. 2003) points to the three groups being part of a monophyletic lineage, as in the diagram on the right.

However all the other studies that I can think of support these three lineages as independent and as a grade diverging prior to the evolution of the tracheophytes.

This phylogenetic relationship was proposed based on morphology, physiology, and biochemistry data (Mishler & Churchill 1984). Then subsequently supported by molecular sequence data (Mishler et al. 1994).

 

Another alternative hypothesis was supported by sporophyte morphological data (Garbary & Renzaglia 1998) and cox3 mitochondrial sequence data (Malek et al. 1996).

So, I think that this could be presented to students as an active scientific example of different data giving conflicting signals. Often science is much messier than we explain to students. They could be presented with multiple alternative hypotheses for these relationships and have to discuss the different scenarios or perhaps the different types of data used for each. 

However, if I only wanted to present one phylogenetic relationship to my students I would go with this one, below. This relationship is supported by Qui et al. (2006), which uses molecular sequence data from the chloroplast, mitochondria and nucleus on over 100 taxa. Others may disagree, but this is the phylogeny that I would recommend using as our most current hypothesis for teaching students about relationships among the bryophytes.

References

Garbary, D. J., K. S. Renzaglia & J. G. Duckett. 1993. The phylogeny of land plants: A cladistic analysis based on male gametogenesis. Plant Systematics and Evolution 188: 237-269.

Garbary, D. J. & K. S. Renzaglia. 1998. Bryophyte phylogeny and the evolution of land plants: Evidence from development and ultrastructure. Pp. 45-63 in J. W. Bates, N. W. Ashton & J. G. Duckett (Editors), Bryology for the Twenty-first Century. Maney Publishing, Leeds.

Kenrick, P. & P. R. Crane. 1997. The Origin and Early Diversification of Land Plants. Smithsonian Institution Press, Washington, D.C.

Malek, O., K. Lättig, R. Hiesel, A. Brennicke & V. Knoop. 1996. RNA editing in bryophytes and a molecular phylogeny of land plants. The European Molecular Biology Organization Journal 15: 1403-1411.

Mishler, B. D. & S. P. Churchill. 1984. A cladistic approach to the phylogeny of "bryophytes." Brittonia 36:406-424.

Mishler, B. D., L. A. Lewis, M. A. Buchheim, K. S. Renzaglia, D. L. Garbary, C. F. Delwiche, F. W. Zechman, T. S. Kantz & R. L. Chapman. 1994. Phylogenetic relationships of the “green algae” and “bryophytes”. Annals of the Missouri Botanical Garden 81: 451-483.

Nishiyama, T., P. G. Wolf, M. Kughita, R. B. Sinclair, M. Sugita, C. Sugiura, T. Wakasugi, K. Yamada, K. Yoshinaga, K. Yamaguchi, K. Euda & M. Hasebe. 2004. Chloroplast phylogeny indicates that bryophytes are monophyletic. Molecular Biology and Evolution 21: 1813-1819.

Qiu, Y.-L., L. Li, B. Wang, Z. Chen, V. Knoop, M. Groth-Malonek, O. Dombrovska, J. Lee, L. Kent, J. Rest, G. F. Estabrook, T. A. Hendry, D. W. Taylor, C. M. Testa, M. Ambros, B. Crandall-Stotler, R. J. Duff, M. Stech, W. Frey, D. Quandt & C. C. Davis. 2006. The deepest divergences in land plants inferred from phylogenomic evidence. Proceedings of the National Academy of Sciences of the USA 103: 15511-15516.

My Bryology Bookshelf - V

Another book that I picked up recently was a great book of fabulous images from Bill and Nancy Malcolm, entitled The Forest Carpet. This book is from the authors of the spectacular bryophyte glossary. They cover all three lineages of bryophytes (liverworts, mosses and hornworts), one lineage of ferns, a couple of fern allies (aka. fern friends), and lichens. The images are large, filling the pages of this coffee-table sized book. Each image comes with an informative caption, identifying the specific species pictured and notes the magnification. There are photos of the plants growing in their particular habitat, closeups of the exterior of the plants, and some sections showing the interior arrangements of the cells.

The goal of this book is to make people aware of the smaller organisms that make up the green background that covers the forest floor like a carpet in New Zealand, hence the title. I think that this book does a great job of immersing you into this miniature world!

Hornworts, A Separate Group?

A few weeks back (My Bryology Bookshelf III) I had a question about when hornworts were moved from being recognized as a type of liverwort to their own independent lineage. I put this question to my lab-mate Juan Carlos and he came up with this response.

Since the flat thalloid gametophyte looks quite similar between hornworts and some liverworts, they were thought to be to be a type of liverwort. They were definitely thought to be unique due to their sporophyte. Hornwort sporophytes grow from the base and open by two longitudinal slits that start from the top and move toward the bottom. The spores line the entire length of the interior of the sporophyte. Whereas liverwort sporophytes consist of a spore filled capsule atop a thin translucent stalk.

One of the first researchers to publicly recognize the hornworts as their own phylum (Anthocerotophyta) was Rothmaler in 1951. So there's the answer to my question. When were hornworts recognized as a separate lineage?

For more information on hornwort classification check out this scientific article.

Raymond E. Stotler and Barbara Crandall-Stotler. 2005. A Revised Classification of the Anthocerotophyta and a Checklist of the Hornworts of North America, North of Mexico. The Bryologist 108:16-26.

My Bryology Bookshelf - III

Mosses With A Hand Lens by A. J. Grout 

Third Edition - 1924

A Popular Guide to the Common or Conspicuous Mosses and Liverworts of the North-Eastern United States

In my search for a field guide to the mosses of New England, I came across this book at my university library. I then purchased my own copy to add to my reference shelf. You can check out the entire book here online at GoogleBooks.

Some great aspects of this book are that it is meant to be used with a hand lens. Other books require either a dissecting or compound microscope. The initial dichotomous key is a manageable length with 25 couplets. Then it spits into Acrocarpous and Pleurocarpous mosses that then have a 36 and 14 couplet key respectively. The line drawings are really well done and are quite informative for species identification. The photographs are ok, especially considering they are from 1924, but are pretty grainy and black & white. The diagrams for the liverworts are typically much smaller and with less detail. This may show a bias of the author toward the mosses.

Since the book is quite old some of the names of the genera are out of date. But it is interesting historically to see how the scientific names have changed from then to now.

Catharinea is now Atrichum

Webera is now Diphyscium

Georgia is now Tetraphis

Another interesting finding in this book is that hornworts are described as a specific type of liverwort. They are classified in the family Anthocerotaceae, The Horned Liverworts. Currently the hornworts are classified as a distinct lineage separate from the liverworts. Thus there are three main groups of Bryophytes; Mosses, Liverworts and Hornworts. I am not sure when hornworts were moved to their own lineage. Sometime between 1924 and now? This is a question for my lab-mate Juan Carlos. I will let you know what he says when I see him tomorrow.   
 

Happy St. Patrick's Day

Shamrocks and leprichauns are green just like mosses. To celebrate the day I dug through my digital photos and came up with some green mossy gems to share. Below is a photo of the moss species that I am working on for my dissertation research, Funaria hygrometrica.

This is another species in the Funariaceae, Physcomitrium pyriforme with sporophytes that have matured and are now brown.

All of these photos were taken a couple of years ago. I initially tried growing my mosses on soil in pots in the greenhouses we have on campus. Unfortunately the mist rooms kept them too moist and the mosses were overrun by cyanobacteria and algae. That is when I switched to growing them in little plastic terrariums on a light cart in my laboratory.

I am not sure which species is below. The leafy gametophytes of members of the Funariaceae all look very similar and I did not mark the photo.

There are a few more photos below the fold. Enjoy!

These are some hornworts that my labmate Juan Carlos had planted up in the greenhouse. From the almost readable label it looks like they might be in the genus Anthoceros.

An additional up close shot of the capsules and calyptra of Funaria hygrometrica.

In this batch of bryophyte images I also took a number of shots of the orchids that grow in our teaching greenhouses. Though they are gaudy angiosperms I thought that I would include a couple of them here.

New Addition to the Goffinet Lab Website

One of my advisors, Dr. Bernard Goffinet, maintains a website for our bryophyte lab group. Recently two classification outlines were added to the website (under the heading Links), one each for mosses and hornworts. For the mosses there is an alphabetical list of all the current genera at the top of the page. By clicking on a genus name you are whisked away to the location of that genus in the overall classification.

If is has been a while since you thought about classification systems for organisms you might need to bust out your favorite old pneumonic device. The one I learned was Kings Play Cards On Fat Green Stools, which usually helps me to remember Kingdom Phylum Class Order Family Genus Species. However the latest classification schemes have added another layer above Kingdom, which is Domain. There are three of these and plants fall into the Domain Eukarya. I won't bore you with the history of how we arrived at this three domain system, but if you are interested the wiki page for biological classification has some good info. So for mosses the upper end of the classification goes something like this...

Domain Eukarya
Kingdom Plantae
Phylum Bryophyta

The online classification starts with Subdivisions, a half step below Phylum, and then continues on from there. Besides Subdivision, there are a couple other classification ranks that may be unfamiliar, but they are pretty intuitive. From this list you can see other closely related genera, closely related families, and so on.

The hornwort classification is maintained by one of my labmates, Juan Carlos Villarreal and it comes with detailed descriptions of the individual genera.

Overall I think that it is a great contribution to have this information out on the web. The classification systems will also be coming out in print in the second edition of Bryophyte Biology, from Cambridge University Press. This book will be available to the public in November. Until then, enjoy this advance version of the classifications.

My First Japanese Bryophyte

Well here I am half way around the world and 13 hours ahead of EST in Connecticut. The flight was incredibly long but the travel went smoothly overall. We are currently staying at the Graduate University of SOKENDAI having a week of orientation where we are taking Japanese language classes and learning about Japanese culture.

I decided to poke around the bushes outside of the university buildings to see if I could find any bryophytes. What I found were some super tiny hornworts with sporophytes. The cluster here is about the size of my fingernail. There are three main groups of plants that are typically called bryophytes: mosses, liverworts and hornworts.

Hornworts have a flat thallus that grows pressed close to the ground. They do not have stems and leaves as mosses do. Many of the features that set hornworts apart from other bryophytes relate to the sporophytes. They have long, skinny sporophytes that produce spores inside for the entire length. They do not have a swollen capsule as in mosses and liverworts. Pictured here are some very young sporophytes peeking out from the wavy edged hornwort.

The spores are released from these structures by a very interesting mechanism. The oldest and most mature spores are located at the tip of the sporophytes. When they are ready to be released there are 1 to 2 lines that open from the top downward like zippers releasing the spores. The sporophyte continues to grow from the bottom making more and more spores that are released as the opening moves toward the bottom.

This phenomenon is where the common name hornworts comes from. After the spores have been released the sporophyte tip which has been divided in half by the lines of dehiscence (aka. zippers) dries and curls. They look like two horns, thus the name Hornwort. These photos do not show this neat phenomenon since the sporophytes are really young. Hornworts occur around the world and we have them in Connecticut too.

Keep your eyes peeled for these curly tipped sporophytes which tell you that you have found a hornwort. It is a good feature to know about when searching for them.