Frederic Lens

Frederick

“I am fascinated by the endless variation of life forms in flowering plants. Why do plants reinvent woodiness that was once lost in their herbaceous ancestors?”

Although I always had been fascinated by animals and plants, I would never have thought I would become an expert in wood anatomy, a field which I (and many others) initially considered “outdated” and “boring”. But now, I cannot disagree more … Basically, I rolled into it, partly because of enthusiastic professors and partly because of my reluctance to experiment on animals. After being in contact to the wonderfull world of evolutionary wood anatomy in my MSc thesis, I decided to do a PhD focusing on the flowering plant order Ericales. In my postdoc period, my internship in the xylem physiology lab of John Sperry (University of Utah, USA) triggered my interest to investigate tree adaptations to drought stress in greater detail. Furthermore, I got fascinated to know more about the genetic mechanism behind wood formation. Wood formation has evolved hundreds of times within flowering plants, but we still do not know what genes underly one of the most fundamental processes on Earth. My anatomical, physiological and molecular work is now combined into an integrative study on secondary woodiness that wants to find out why and how predominantly herbaceous plant groups become woody again.

Career

I started my career in the university of Leuven (Belgium) where I carried out my studies (1995-1999), my PhD (2000-2005), and a few years as postdoc fellow (2006-2010). Since 2010, I was applied by the University of Leiden as tenure tracker in wood anatomy, and few years later (2013) I was transferred to Naturalis Biodiversity Center where I have obtained a tenured position.

Research interest

My research interest is to understand why herbaceous species on islands and other parts in the world have developed into woody shrubs, and to find out what is the molecular mechanism that has triggered this evolutionary habit shift in various lineages of flowering plants. This long-standing evolutionary phenomenon dates back to Darwin’s voyage on board the H.M.S. Beagle, and is known in the literature as insular woodiness or secondary woodiness. I am tackling both main questions applying an ‘eco-evo-devo’ approach, which integrates water flow measures in stems and detailed anatomical observations allowing to investigate structure-function relationships in stems, together with state-of-the-art transcriptome experiments and niche modelling.

Current research topics

Is insular woodiness triggered by drought stress on the Canary Islands?

Assessing why various groups of herbaceous flowering plants have reversed to the ancestral woody habit condition is a complex question involving various environmental and abiotic factors, and it may depend on the group under study. For the Canary Island flora, we have identified at least 220 insular woody species derived from 38 flowering plant groups that have evolved independently from each other. Most of the insular woody species grow in the dry coastal regions of the Canary Islands, suggesting a link between drought stress and wood formation. This link is also evident based on an ongoing review project where I am compiling a list of secondarily woody species within angiosperms (over 4500 species found so far). Using water flow measurements in stems, I am investigating whether stems of insular woody species can avoid air bubbles (embolisms) inside water conducting cells to a much better extent than the stems of their herbaceous relatives, which is known to be a good proxy for drought resistance. I am also interested to investigate which anatomical stem features underlie the differences in embolism resistance. These anatomical and physiological observations are combined to a molecular dating approach assessing whether the origin of the insular woody groups coincided with dry paleoclimatic periods. Also niche modelling analyses are being carried out to assess whether the insular woody species have a “drier” niche compared to the other species on the Canary Islands.

More information: Lens et al 2013 (Canary Island review, and embolism resistance review).

Structure-function relationships in woody and herbaceous plants

First of all, I am interested to find out whether stems of secondarily woody species are more resistant to embolism formation than stems of herbaceous relatives. As a proof-of-principle, we compared hydraulic failure in a herbaceous wild-type and a woody mutant of Arabidopsis thaliana by measuring the pressure inducing 50% loss of hydraulic conductance (P50).

The water transport pipeline in herbs is assumed to be more vulnerable to drought than in trees due to the formation of frequent embolisms (gas bubbles), which could be removed by the occurrence of root pressure, especially in grasses. In a recent study (Lens et al 2016), we studied hydraulic failure in herbaceous angiosperms by measuring P50 in stems of 26 species – mainly European grasses (Poaceae). Our measurements show a large range in P50 from -0.5 to -7.5MPa, which overlaps with 94% of the woody angiosperm species in a worldwide, published dataset (Choat et al 2012), and which strongly correlates with an aridity index. Moreover, the P50 values obtained were substantially more negative than the midday water potentials for five grass species monitored throughout the entire growing season, suggesting that embolism formation and repair are not routine and mainly occur under water deficits. These results show that both herbs and trees share the ability to withstand very negative water potentials without embolism formation in their xylem conduits during drought stress.

In addition, structure-function trade-offs in grass stems reveal that more resistant species are more lignified, which was confirmed for herbaceous and closely related woody species of the daisy group (Asteraceae). Our findings could imply that herbs with more lignified stems will become more abundant in future grasslands under more frequent and severe droughts, potentially resulting in lower forage digestibility.

Our paper on seven closely related woody Acer taxa (not secondarily woody) with a difference in embolism resistance was one of the first studies that combines in-depth wood anatomical observations with hydraulic measures to investigate structure-function relationships in wood. The main highlights of this study is that fine-scale intervessel pit structures play a crucial role in the water transport pathway of woody plants (see picture), and that a combination of different characters are able reach a certain level of embolism resistance.

More information: Lens et al 2011 (Acer publication), Lens et al 2013 (embolism resistance review).

Unravelling the molecular wood pathway leading to insular woodiness

We are performing detailed transcriptome experiments in Arabidopsis thaliana and Brassica oleracea using RNA-seq of different developmental stages of the stem that are important to wood formation, i.e. herbaceous stage, cambium stage and wood stage. Using these two case studies in Brassicaceae, we are searching for key regulatory genes initiating cambium and wood formation, and the transcriptome datasets will provide the basis for future planned studies that want to infer whether shifts towards secondary woodiness in other families have been triggered by a common molecular pathway or whether there are major differences in the way how wood-forming genes are turned on.

In the Melzer et al (2008) paper, we published the most woody mutant of Arabiopsis published so far, in which the two flowering time control genes SOC1 and FUL were knocked out. We have built on this publication, and recently published a comparative transcriptome paper including different developmental stem stages, and leaf stages as an internal control (Davin et al 2016).

We did not found evidence for the presence of only one ‘master gene’ that would turn on the wood pathway in the woody mutant. Instead, most of the hundreds of genes differentially expressed between crucial stem developmental stages were closely linked into a dense gene network. We interpreted this gene network as an alternative mechanism to explain the apparent simple genetic trigger causing rampant evolutionary transitions towards secondary woodiness. If these networks are conserved amongst plant lineages, we may assume that modification of multiple genes within the network could lead to wood formation. In other words, not just a single master gene, but several regulatory genes embedded into a shared gene interaction network could be responsible for all these convergent habit shifts to woody life forms.

Co-promotor/supervisor

Davin N. Evolution of secondary woodiness: driver of island plant radiations? University of Leiden, PhD defense foreseen at end of 2016.

Chacon Dória L. A xylem physiological approach to better understand insular woodiness – is drought stress involved? University of Leiden, PhD defense foreseen mid 2019.

Courses

Since 2010 I am involved in the courses Evolution in angiosperms (part wood anatomy; BSc level), Biodiversity of Plants (part anatomy of stems, roots and leaves; BSc level), Evolutionary Developments (integrated wood anatomy; BSc level), and Trends in Evodevo (part insular woodiness; MSc level), all at Leiden University.