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Tropical trees are living time capsules of human history

By | Forestry, Global Collaborations, News, Plant Science

Tropical forest trees are the centerpiece of debates on conservation, climate change and carbon sequestration today. While their ecological importance has never been doubted, what has often been ignored is their ability to store cultural heritage. Using recent advances in scientific methods and a better understanding of the growth of these trees, researchers can now uncover, in detail, the growing conditions, including human management, that have occurred around these ancient giants over their centuries-long life span.

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Chang Min SHIN / Pixabay

What’s the story Morning Glory? Taxonomy, evolution and sweet potatoes

By | Agriculture, Botany, Fruits and Vegetables, News

Scientists at the University of Oxford reveal that the sweet potato and its storage root originated at least 2 million years ago — that is, not only before agriculture but also long before modern humans appeared on Earth.

The scientists’ research indicates that the storage root was an already-existing trait that predisposed the plant for cultivation and not solely the result of human domestication, as previously thought. This discovery, published in Nature Plants, is part of a comprehensive monographic study of the morning glories, the biggest study of this group of plants to date, which also contributes important insights to the taxonomy and evolution of this megadiverse group of plants.

The researchers also discovered that sweet potato is not the only species of morning glory that produces storage roots. In fact at least 62 other species in the group also produce these underground organs, some of them as big as those of the sweet potato and many also edible.

Dr Pablo Muñoz, from Oxford‘s Department of Plant Sciences, whose PhD thesis formed a significant part of the paper, said: ‘Most other studies trying to understand the evolution of the sweet potato assumed that its storage root is a product of domestication by humans whereas this study demonstrates that storage roots evolved many times independently in different species including sweet potato before humans.’

The plant genus Ipomoea, commonly known as morning glories, is one of the largest groups of flowering plants in the world. It includes over 800 species, including many ornamental plants and one of the most important crops for human consumption: the sweet potato (Ipomoea batatas). However, despite their importance and widespread distribution, most species of morning glories are very poorly known and have never been studied across their entire geographical range, hindering the understanding of this important group of plants.

Researchers at the University of Oxford’s Department of Plant Sciences have led the first comprehensive monographic study of the morning glories at a global scale. It is a long-term collaboration with colleagues at the International Potato Center, in Peru, Oregon State and Duke Universities in the US and the Royal Botanic Garden Edinburgh. Their results include the description of 63 new species (almost 10% of the species known in the whole genus) and the identification of a large number of synonyms — entities described in different places under different names that are, in reality, the same species.

Their methods could offer a solution to the massive backlog in documenting and describing the bulk of the world’s plant species.

The scientists demonstrate how a monographic taxonomic study, carried out at a global scale, can make massive contributions to our understanding of the diversity existing in poorly known groups of organisms. By working out the evolution of the morning glories, they were also able to investigate several questions pertaining to the origin and evolution of the sweet potato.

The research uses herbarium specimens — dried plants preserved in botanical gardens, museums and other institutions — for both morphological comparative studies and molecular analyses. Herbarium specimens constitute an unparalleled resource with which to address the study of inadequately known groups of plants and is the only feasible way to study megadiverse tropical groups across their entire distribution.

Lead author, Professor Robert Scotland, said: ‘We hope this study acts as a catalyst in demonstrating the scale of progress that can be achieved. Taxonomy has often been perceived as a merely descriptive science, a continuation of the work carried out by 18th and 19th century naturalists and no longer necessary.

‘However, we believe that an accurate, up-to-date taxonomy is necessary to tackle the biodiversity crisis. A large percentage of tropical plant species are so poorly known that, in practice, they are invisible to conservation studies. Taxonomy is the science that underpins biology and provides our basic knowledge of what species there are and where they live. Our study demonstrates the potential of taxonomy, through the integration of morphological studies and molecular analyses, to contribute to understanding much of the plant diversity existing on Earth.’

Professor Robert Scotland said

Read the paper: Nature Plants

Article source: University of Oxford

Image credit: Chang Min SHIN / Pixabay

Scientists present new data on the evolution of plants and the origin of species

By | News, Plant Science

There are over 500,000 plant species in the world today. They all evolved from a common ancestor. How this leap in biodiversity happened is still unclear. An international team of researchers presents the results of a unique project on the evolution of plants. Using genetic data from 1,147 species the team created the most comprehensive evolutionary tree for green plants to date.

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2016 Plant Science Round Up

By | Blog, Research

Another fantastic year of discovery is over – read on for our 2016 plant science top picks!

January

Zostera marina

A Zostera marina meadow in the Archipelago Sea, southwest Finland. Image credit: Christoffer Boström (Olsen et al., 2016. Nature).

The year began with the publication of the fascinating eelgrass (Zostera marina) genome by an international team of researchers. This marine monocot descended from land-dwelling ancestors, but went through a dramatic adaptation to life in the ocean, in what the lead author Professor Jeanine Olsen described as, “arguably the most extreme adaptation a terrestrial… species can undergo”.

One of the most interesting revelations was that eelgrass cannot make stomatal pores because it has completely lost the genes responsible for regulating their development. It also ditched genes involved in perceiving UV light, which does not penetrate well through its deep water habitat.

Read the paper in Nature: The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea.

BLOG: You can find out more about the secrets of seagrass in our blog post.

 

February 

Plants are known to form new organs throughout their lifecycle, but it was not previously clear how they organized their cell development to form the right shapes. In February, researchers in Germany used an exciting new type of high-resolution fluorescence microscope to observe every individual cell in a developing lateral root, following the complex arrangement of their cell division over time.

Using this new four-dimensional cell lineage map of lateral root development in combination with computer modelling, the team revealed that, while the contribution of each cell is not pre-determined, the cells self-organize to regulate the overall development of the root in a predictable manner.

Watch the mesmerizing cell division in lateral root development in the video below, which accompanied the paper:


Read the paper in Current Biology: Rules and self-organizing properties of post-embryonic plant organ cell division patterns.

 

March

In March, a Spanish team of researchers revealed how the anti-wilting molecular machinery involved in preserving cell turgor assembles in response to drought. They found that a family of small proteins, the CARs, act in clusters to guide proteins to the cell membrane, in what author Dr. Pedro Luis Rodriguez described as “a kind of landing strip, acting as molecular antennas that call out to other proteins as and when necessary to orchestrate the required cellular response”.

Read the paper in PNAS: Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling.

*If you’d like to read more about stress resilience in plants, check out the meeting report from the Stress Resilience Forum run by the GPC in coalition with the Society for Experimental Biology.*

 

April

Arbuscular mycorrhizal fungi.

This plant root is infected with arbuscular mycorrhizal fungi. Image credit: University of Zurich.

In April, we received an amazing insight into the ‘decision-making ability’ of plants when a Swiss team discovered that plants can punish mutualist fungi that try to cheat them. In a clever experiment, the researchers provided a plant with two mutualistic partners; a ‘generous’ fungus that provides the plant with a lot of phosphates in return for carbohydrates, and a ‘meaner’ fungus that attempts to reduce the amount of phosphate it ‘pays’. They revealed that the plants can starve the meaner fungus, providing fewer carbohydrates until it pays its phosphate bill.

Author Professor Andres Wiemsken explains: “The plant exploits the competitive situation of the two fungi in a targeted manner, triggering what is essentially a market-based process determined by cost and performance”.

Read the paper in Ecology Letters: Options of partners improve carbon for phosphorus trade in the arbuscular mycorrhizal mutualism.

 

May

The transition of ancient plants from water onto land was one of the most important events in our planet’s evolution, but required a massive change in plant biology. Suddenly plants risked drying out, so had to develop new ways to survive drought.

In May, an international team discovered a key gene in moss (Physcomitrella patens) that allows it to tolerate dehydration. This gene, ANR, was an ancient adaptation of an algal gene that allowed the early plants to respond to the drought-signaling hormone ABA. Its evolution is still a mystery, though, as author Dr. Sean Stevenson explains: “What’s interesting is that aquatic algae can’t respond to ABA: the next challenge is to discover how this hormone signaling process arose.”

Read the paper in The Plant Cell: Genetic analysis of Physcomitrella patens identifies ABSCISIC ACID NON-RESPONSIVE, a regulator of ABA responses unique to basal land plants and required for desiccation tolerance.

 

June

Knoblauch with phloem

Professor Michael Knoblauch shows off a microscope image of phloem tubes. Image credit: Washington State University.

Sometimes revisiting old ideas can pay off, as a US team revealed in June. In 1930, Ernst Münch hypothesized that transport through the phloem sieve tubes in the plant vascular tissue is driven by pressure gradients, but no-one really knew how this would account for the massive pressure required to move nutrients through something as large as a tree.

Professor Michael Knoblauch and colleagues spent decades devising new methods to investigate pressures and flow within phloem without disrupting the system. He eventually developed a suite of techniques, including a picogauge with the help of his son, Jan, to measure tiny pressure differences in the plants. They found that plants can alter the shape of their phloem vessels to change the pressure within them, allowing them to transport sugars over varying distances, which provided strong support for Münch flow.

Read the paper in eLife: Testing the Münch hypothesis of long distance phloem transport in plants.

BLOG: We featured similar work (including an amazing video of the wound response in sieve tubes) by Knoblauch’s collaborator, Dr. Winfried Peters, on the blog – read it here!

 

July

Ancient barley grain

Preserved remains of rope, seeds, reeds and pellets (left), and a desiccated barley grain (right) found at Yoram Cave in the Judean Desert. Credit: Uri Davidovich and Ehud Weiss.

In July, an international and highly multidisciplinary team published the genome of 6,000-year-old barley grains excavated from a cave in Israel, the oldest plant genome reconstructed to date. The grains were visually and genetically very similar to modern barley, showing that this crop was domesticated very early on in our agricultural history. With more analysis ongoing, author Dr. Verena Schünemann predicts that “DNA-analysis of archaeological remains of prehistoric plants will provide us with novel insights into the origin, domestication and spread of crop plants”.

Read the paper in Nature Genetics: Genomic analysis of 6,000-year-old cultivated grain illuminates the domestication history of barley.

BLOG: We interviewed Dr. Nils Stein about this fascinating work on the blog – click here to read more!

 

August

Another exciting cereal paper was published in August, when an Australian team revealed that C4 photosynthesis occurs in wheat seeds. Like many important crops, wheat leaves perform C3 photosynthesis, which is a less efficient process, so many researchers are attempting to engineer the complex C4 photosynthesis pathway into C3 crops.

This discovery was completely unexpected, as throughout its evolution wheat has been a C3 plant. Author Professor Robert Henry suggested: “One theory is that as [atmospheric] carbon dioxide began to decline, [wheat’s] seeds evolved a C4 pathway to capture more sunlight to convert to energy.”

Read the paper in Scientific Reports: New evidence for grain specific C4 photosynthesis in wheat.

 

September

CRISPR lunch

Professor Stefan Jansson cooks up “Tagliatelle with CRISPRy fried vegetables”. Image credit: Stefan Jansson.

September marked an historic event. Professor Stefan Jansson cooked up the world’s first CRISPR meal, tagliatelle with CRISPRy fried vegetables (genome-edited cabbage). Jansson has paved the way for CRISPR in Europe; while the EU is yet to make a decision about how CRISPR-edited plants will be regulated, Jansson successfully convinced the Swedish Board of Agriculture to rule that plants edited in a manner that could have been achieved by traditional breeding (i.e. the deletion or minor mutation of a gene, but not the insertion of a gene from another species) cannot be treated as a GMO.

Read more in the Umeå University press release: Umeå researcher served a world first (?) CRISPR meal.

BLOG: We interviewed Professor Stefan Jansson about his prominent role in the CRISPR/GM debate earlier in 2016 – check out his post here.

*You may also be interested in the upcoming meeting, ‘New Breeding Technologies in the Plant Sciences’, which will be held at the University of Gothenburg, Sweden, on 7-8 July 2017. The workshop has been organized by Professor Jansson, along with the GPC’s Executive Director Ruth Bastow and Professor Barry Pogson (Australian National University/GPC Chair). For more info, click here.*

 

October

Phytochromes help plants detect day length by sensing differences in red and far-red light, but a UK-Germany research collaboration revealed that these receptors switch roles at night to become thermometers, helping plants to respond to seasonal changes in temperature.

Dr Philip Wigge explains: “Just as mercury rises in a thermometer, the rate at which phytochromes revert to their inactive state during the night is a direct measure of temperature. The lower the temperature, the slower phytochromes revert to inactivity, so the molecules spend more time in their active, growth-suppressing state. This is why plants are slower to grow in winter”.

Read the paper in Science: Phytochromes function as thermosensors in Arabidopsis.

 

November

Ginkgo

A fossil ginkgo (Ginkgo biloba) leaf with its modern counterpart. Image credit: Gigascience.

In November, a Chinese team published the genome of Ginkgo biloba¸ the oldest extant tree species. Its large (10.6 Gb) genome has previously impeded our understanding of this living fossil, but researchers will now be able to investigate its ~42,000 genes to understand its interesting characteristics, such as resistance to stress and dioecious reproduction, and how it remained almost unchanged in the 270 million years it has existed.

Author Professor Yunpeng Zhao said, “Such a genome fills a major phylogenetic gap of land plants, and provides key genetic resources to address evolutionary questions [such as the] phylogenetic relationships of gymnosperm lineages, [and the] evolution of genome and genes in land plants”.

Read the paper in GigaScience: Draft genome of the living fossil Ginkgo biloba.

 

December

The year ended with another fascinating discovery from a Danish team, who used fluorescent tags and microscopy to confirm the existence of metabolons, clusters of metabolic enzymes that have never been detected in cells before. These metabolons can assemble rapidly in response to a stimulus, working as a metabolic production line to efficiently produce the required compounds. Scientists have been looking for metabolons for 40 years, and this discovery could be crucial for improving our ability to harness the production power of plants.

Read the paper in Science: Characterization of a dynamic metabolon producing the defense compound dhurrin in sorghum.

 

Another amazing year of science! We’re looking forward to seeing what 2017 will bring!

 

P.S. Check out 2015 Plant Science Round Up to see last year’s top picks!

1000 Plants

By | Blog, Interviews

The 1000 plants initiative (1KP) is a multidisciplinary consortium aiming to generate large-scale gene sequencing data for over 1000 species of plants. Included in these species are those of interest to agriculture and medicines, as well as green algae, extremophytes and non-flowering plants. The project is funded by several supporters, and has already generated many published papers.

Gane Wong is a Professor in the Faculty of Science at the University of Alberta in Canada. Having previously worked on the Human Genome Project, he now leads the 1KP initiative. Dennis Stevenson, Vice President for Botanical Research, New York Botanical Garden, and Adjunct Professor, Cornell University (USA), studies the evolution and classification of the Cycadales. He became involved in the 1KP initiative as an opportunity to sample the breadth of green plant diversity.

We spoke to both Professor Stevenson (DS) and Professor Wong (GW) about the initiative. Professor Douglas Soltis from Florida Museum of Natural History also contributed to this blog post with input in editing the answers.

What do you think has been the biggest benefit of 1KP?

DS: This has been an unparalleled opportunity to reveal and understand the genes that have led to the plant diversity we see around us. We were able to study plants that were pivotal in terms of plant evolution but which have not previously been included in sequencing projects as they are not considered important economically

The 1KP project presented a fantastic opportunity to explore plant biodiversity. Photo by Bob Leckridge. Used under Creative Commons 2.0.

The 1KP project presented a fantastic opportunity to explore plant biodiversity. Photo by Bob Leckridge. Used under Creative Commons 2.0.

GW: The project was funded by the Government of Alberta and the investment firm Musea Ventures to raise the profile of the University of Alberta. Notably there was no requirement by the funders to sequence any particular species. I was able to ask the plant science community what the best possible use of these resources would be. The community was in full agreement that the money should be used to sample plant diversity.

Hopefully our work will change the thinking at the funding agencies regarding the value of sequencing biodiversity.

What techniques were utilized in this project to carry out the research?

GW: Complete genomes were too expensive to sequence. Many plants have unusually large genomes and de novo assembly of a polyploid genome remains difficult. To overcome this problem, we sequenced transcriptomes. However, this made our sample collection more difficult as the tissue had to be fresh. In addition, when we started the project, the software to assemble de novo transcriptomes did not work particularly well. I simply made a bet that these problems would be solved by the time we collected the samples and extracted the RNA. For the most part that’s what happened, although we did end up developing our own assembly software as well!

The 1KP initiative is an international consortium. How has the group evolved over time and what benefits have you seen from having this diverse set of skills?

GW: 1KP would not be where it is today without the participation of scientists around the world from many different backgrounds. For example, plant systematists who defined species of interest and provided the tissue samples worked alongside bioinformaticians who analyzed the data, and gene family experts who are now publishing fascinating stories about particular genes.

 DS: One of the great things about this project is how it has evolved over time as new researchers became involved. There is no restriction on who can take part, which species can be studied or which questions can be asked of the data. This makes the 1KP initiative unique compared to more traditionally funded projects.

GW: We continually encouraged others to get involved and mine our data for interesting information. We did a lot of this through word of mouth and ended up with some highly interesting, unexpected discoveries. For example, an optogenetics group at MIT and Harvard used our data to develop new tools for mammalian neurosciences. This really highlights the importance of not restricting the species we study to those of known economic importance.

According to ISI outputs from this research, two of the most highly cited papers from 1KP are here and here.

You aimed to investigate a highly diverse array of plants. How many plants of the major phylogenetic groups have now been sequenced, and are you still working on expanding the data set?

DS: A lot of thought went into the species selection. We aimed for proportional representation (by number of species) of the major plant groups. We also aimed to represent the morphological diversity of those groups.

GW: Altogether, we generated 1345 transcriptomes from 1174 plant species.

Has this project lead to any breakthroughs in our understanding of the phylogeny of plants?

DS: This will be the first broad look at what the nuclear genome has to tell us, and the first meaningful comparison of large nuclear and plastid data sets. However, due to rapid evolution plus extinction, many parts of the plant evolutionary tree remain extremely difficult to solve.

Hornworts are non-vascular plants that grow in damp, humid places. Photo by Jason Hollinger. Used under Creative Commons License 2.0.

Hornworts are non-vascular plants that grow in damp, humid places. Photo by Jason Hollinger. Used under Creative Commons License 2.0.

One significant breakthrough was the discovery of horizontal gene transfer from a hornwort to a group of ferns. This was unexpected and very interesting in terms of the ability of those ferns to be able to accommodate understory habitats.

GW: With regard to horizontal gene transfer, there are papers in the pipeline that will illustrate the discovery of even more of these events in other species. We have also studied gene duplications at the whole genome and gene family level. This is the most comprehensive survey ever undertaken, and people will be surprised at the scale of the discoveries. However, we will be releasing our findings shortly as part of a series and it would be unwise for us to give the story away here! Keep a look out for these!

Interview with Dr. Winfried Peters: Bringing forgotten ideas on plant biomechanics into the 21st century

By | Blog, Interviews

This week we spoke to Dr. Winfried S. Peters from Indiana University/Purdue University Fort Wayne (IPFW). His research mainly focuses on the biomechanics of plant cells, which led him to take a second look at some of the ideas of botanists in the 19th and early 20th century and use modern techniques to make exciting new discoveries.

Winfried Peters

Dr Winfried S. Peters, Indiana University/Purdue University Fort Wayne (IPFW), next to several tons of land-plant sieve elements!

 

Could you begin by describing your research interests?
I am interested in the biophysical aspects of the physiology of plants and animals. In plants, my research focuses on the mechanics of growth and morphogenesis, and on the cell biology of long-distance transport in the phloem. For both topics, a solid background in the history of the field can be quite helpful – I love studying the old literature to reconstruct the ideas botanists had a century or two ago regarding the functioning of plants.

At the recent New Phytologist Symposium, entitled “Colonization of the terrestrial environment 2016”, you presented fascinating work on the sieve tubes of kelp, which resemble the phloem tubes of vascular plants. What is the purpose of these tubes?
In large photosynthetic organisms, not all parts of the body are truly autototrophic. Some tissues produce more material by photosynthesis than they need, while others produce less than they require or none at all– think of green leaves and growing root tips. Over-producing tissues can act as sources and export photoassimilates to needy sink tissues. Sieve tubes are arrays of tubular cells that mediate this exchange, enabling the rapid movement of photosynthate-rich cytoplasm between sources and sinks.

What techniques did you utilize to investigate the function of these tubes, and what did this reveal?
During my recent sabbatical, I became involved in this project in the lab of my friend and long-term collaborator, Professor Michael Knoblauch. Michael heads the Franceschi Microscopy and Imaging Center at Washington State University, where we studied sieve tubes of the Bull Kelp (Nereocystis luetkeana) using a variety of state-of-the-art microscopy techniques. Most importantly, we employed fluorescent dyes to visualize transport in sieve tube networks. To do this, one needs to work with intact kelp, which is demanding given a thallus size of 12 meters and more. So we moved to Bamfield Marine Sciences Centre on Vancouver Island, where Bull Kelp is a ‘common weed’.

A particularly important result was the pressure-induced reversal of the flow direction in sieve tubes and across sieve plates. This was in line with Ernst Münch’s (1876-1946) theory, who suggested that sieve tube transport was driven by osmotically generated pressure gradients.

 

Nereocystis wounding

An intact Nereocystis luetkeana is kept in a tank (right) while sieve tube transport is studied using a fluorescence microscope. Photo credit: Michael Knoblauch.

How do the biomechanics of the kelp sieve tubes differ from the phloem tubes of higher plants?
Regarding cytoplasmic translocation, there doesn’t seem to be a difference – in higher plants as in kelps, the contents of the sieve tubes move in bulk flow – but wounding responses differ drastically. After wounding, we found that kelps have a massive swelling of the walls, which reduced the sieve tube diameter by more than 70%. By injecting silicon oil into severed kelp sieve tubes we demonstrated that wall swelling was fully reversible, and that the swelling state of the walls depended on intracellular pressure.

Wounding response in kelp

Sieve wall tubes swell after wounding due to changes in intracellular pressure. (Images taken from video below).

Have reversible wall-swelling reactions been observed in other species, and what are the implications of this finding?
We have observed the wall-swelling response in all kelp species examined. Ironically, there is no shortage of drawings and photographs of kelp sieve tubes with swollen walls in the literature over the last 130 years; however, the dynamics of cell behavior remained hidden in plain sight because fixed tissue samples rather than fully functional, whole organisms were studied. Consequently, sieve tubes with swollen walls were misinterpreted as senescent cells. There also are publications on turgor-dependent cell wall swelling in red and green algae, but these ceased around 1930.

Afterwards, wall swelling was completely forgotten, judging from the textbooks. This is remarkable, as Wilhelm Hofmeister (1824-1877), often celebrated as a founding father of plant biomechanics, denied a significant role for osmotic processes in the generation of turgor, the hydrostatic pressure within plant cells. Rather, he maintained that living cells were pressurized by the swelling of their walls. The example of the kelp sieve tube shows how easy it is to remain unaware of wall swelling when it happens right before our eyes. Maybe we should take Hofmeister’s idea seriously once again?

What are the evolutionary implications of your work?
Brown algae and vascular (land) plants are only remotely related, and their sieve tube networks certainly evolved independently of each other. It seems surprising that such sophisticated structures, which serve a complex function that integrates the physiology of the entire organism, have evolved at least twice, but think again. Real cells are not embedded in a totally homogeneous environment, and neither is the cytoplasm within the cell a homogeneous solution. Thus every cell experiences gradients of solute concentrations along its inner and/or outer surface. As a consequence, differential water fluxes across the plasma membrane will occur, resulting in movements of the cell contents. In other words, Münch flow, the cytoplasmic bulk flow driven by osmotically generated pressure gradients, is not a peculiar process operating specifically in sieve tubes, but a ubiquitous phenomenon. Sieve tubes consist of cells that simply do the things cells do, just a little more efficiently as usual. In this view, the repeated convergent evolution of sieve tube networks is not really unexpected.

But kelps resemble land plants in other ways too. As in land plants, kelp cell walls are made of cellulose (at least partly), kelp cells are connected through plasmodesmata, and the kelp life-cycle is a sporophyte-dominated alternation of generations. Evidently, none of these features represents a specific adaptation to life on dry land.


Wound responses including wall swelling in a sieve tube of Nereocystis luetkeana. (Watch for the rapid cell wall swelling between 11 and 14 seconds in!) This video was taken by Professor Michael Knoblauch in collaboration with Dr Winfried S. Peters.
 


If you’d like to know more about this fascinating work, it was been published in the following articles:

Knoblauch, J., Peters, W.S. and Knoblauch, M., 2016. The gelatinous extracellular matrix facilitates transport studies in kelp: visualization of pressure-induced flow reversal across sieve platesAnnals of Botany117(4), pp.599-606.

Knoblauch, J., Drobnitch, S.T., Peters, W.S. and Knoblauch, M., 2016. In situ microscopy reveals reversible cell wall swelling in kelp sieve tubes: one mechanism for turgor generation and flow control? Plant, Cell and Environment39(8), pp.1727-1736.