Jump to content Jump to navigation

Frederic Lens

Dr. F.P. (Frederic) Lens, Assistant Professor - Understanding Evolution

Contact

Email: frederic.lens@naturalis.nl
Phone: +31 (0)6 83172643
Room number: Vondellaan 55, 3rd floor
“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never have thought I would become an expert in wood anatomy, a field which I (and many others) initially considered "outdated" and "boring".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 wunderfull 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 carreer 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

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.

https://science.naturalis.nl/media/medialibrary/2014/08/daisy_lineage.jpg

Example of insular woodiness in the daisy group (Asteraceae) where woody Argyranthemum species native to Macaronesia (left) are derived from herbaceous daisies native to the European mainland (right). The Leucanthemum species is proudly presented by my collaborator dr. Sylvain Delzon (Univ. of Bordeaux, France).

Keywords

insular woodiness, xylem physiology, molecular wood pathway, secondary woodiness, flowering plants, wood anatomy

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)

https://science.naturalis.nl/media/medialibrary/2014/08/Echium_1.jpg
Based on molecular phylogenies, we know that herbaceous Echium species of the European continent have reached the Canary Islands and developed into woody shrubs (redrawn from Böhle et al 1996).

 

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).

https://science.naturalis.nl/media/medialibrary/2016/08/Arabidopsis_VCs.jpg

Vulnerability curves showing xylem vulnerability to embolism between stems of a woody mutant of Arabidopsis and a herbaceous wild-type. The mutant stems have a P50 value of -3.5MPa, which is 1MPa more negative than that of the wild-type. In other words, stems of the (secondarily) woody mutant are more resistant to embolism formation than its herbaceous progenitor, and this difference is significant (adapted from Lens et al 2013, embolism review).

 

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.https://science.naturalis.nl/media/medialibrary/2016/08/range_in_P50_website.jpg

P50 values of (mainly herbaceous) species measured in Lens et al (2016). The range in P50 among the 22 grass species studied varies from -0.5 up to -7.5MPa, largely corresponding with the P50 variation observed in woody angiosperms. Light green bars indicate grasses (Poaceae), dark green bars represent herbaceous eudicots and the orange ones are woody eudicot shrubs that have evolved from some of the herbaceous relatives studied (*daisy lineage, **gentian lineage). Each bar represents the average value for three specimens of the same species and error bars show SE (taken from Lens et al 2016).

 

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. 

https://science.naturalis.nl/media/medialibrary/2016/08/grasses_anatomy.jpg

Cross sections of hollow stems through the internodes of the grasses Phalaris arundinacea (A, P50 = -0.5MPa), Lolium perenne (B, P50 = -4.6MPa), and Brachypodium pinnatum (C, P50 = -6.2MPa), showing more lignification in the outer zones of the stems (arrows), and thicker-walled fibres (inserts) with increasing P50 (taken from Lens et al 2016).

 

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)

https://science.naturalis.nl/media/medialibrary/2014/08/Interconduit_pits.jpg

Interconduit pits showing torus-margo pit membranes in gymnosperms (top row) and homogeneous pit membranes in angiosperms (middle and bottom rows). A: pit membranes in a relaxed state facing no hydraulic stress. B: drought increases the presssure difference between the water-filled and the embolized conduit, potentially allowing air-seeding among adjacent conduits. C: adaptations in pit quality characters can prevent air-seeding to a certain threshold, such as an increased tori-pit aperture ratio in gymnosperms (top), and highly developed vestures (middle) or thicker pit membranes in angiosperms (bottom). Taken from 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.

https://science.naturalis.nl/media/medialibrary/2014/08/Molecular_mechanism.jpg

Is there a common genetic mechanism leading to secondary woodiness in various angiosperm groups with different woody life forms and habitats? From left to right: Argyroxyphium sandwicense (Asteraceae), a rosette tree native to dry high altitude habitats in Hawaii; Descurainia bourgeauana (Brassicaceae), a shrub endemic to the dry Teide vulcano flanks in Tenerife; new species of Begonia (Begoniaceae) growing in the wet Crocker Range (Sabah, Borneo).

 

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). Our sampling strategy is illustrated below:

https://science.naturalis.nl/media/medialibrary/2016/08/sampling_strategy_Arabidopsis.jpg

Sampling strategy and cross-sections of Arabidopsis thaliana soc1-6 ful-7 double mutant (a) and WT samples (b) selected for RNA sequencing. Pictures c and f correspond to cross sections of the herbaceous stems stage (H) of the mutant and the wild-type, respectively; d and e refer to the cambium stem stage (C), and e is a cross section of the wood stage in a relatively young mutant (W). Arrows indicate a complete vascular cambium ring. Asterisks indicate vascular bundle regions. ‘X’ indicates secondary xylem (see Davin et al 2016 for more details).

 

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.

 https://science.naturalis.nl/media/medialibrary/2016/08/wood_formation_network_website.jpg

Interaction network of genes differentlally expressed between the cambium stage and the wood stem stage in the Arabidopsis mutant. Each node represents a differentially expressed gene, lines show interactions following the STRING v10 global Arabidopsis network, and colours indicate clusters of genes that are linked stronger to each other than to other parts of the network (see Davin et al 2016 for more details).

 

Collaborations

-Naturalis Research Group Understanding Evolution: website.

-labs of Sylvain Delzon, Hervé Cochard and Steven Jansen.

-Executive Secretary of International Association of Wood Anatomists (IAWA, 2011-2016): website.

-Associate editor International Association of Wood Anatomists Journal (2009-current) and Journal of Plant Hydraulics (2014-current).

-Member Advisory Board of New Phytologist from 2013-current, section Physiology & Development.

-Management Committee representative for the Netherlands in COST-FP1106 action, entitled ‘STReESS – Studying Tree Responses to extreme Events: a Synthesis’: website.

-TRY initiative (PI Jens Kattge): website.

-Member of Expert Group Meeting on Timber Analysis, organised by United Nations Office on Drugs and Crime.

-Member of Bark Committee.

-Xylem Functional Traits database (PIs Steven Jansen & Brendan Choat); see Choat et al 2012.

-The Kinabalu – Crocker Range Expedition is a joint Sabah Parks and Naturalis Biodiversity Center expedition.

-International Lecythidaceae network (PI Scott Mori): website.

Collections

Scientific wood collection of Naturalis Biodiversity Center, one of the largest comprising about 125.000 wood specimens and over 50.000 wood slides. 

Supervision PhDs

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.

Teaching

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.

Supervision MSc Students

2015 Supervisor - Zaini N.H. - Stem anatomy and growth habit evolution of Asian Begonia (Begoniaceae).
2015 co-supervision MSc thesis - Schellenberg M. - Evolution of secondary woodiness in selected Brassicaceae groups based on global-scale climate niche modeling
2014 Supervisor - Chauvin T. - Xylem anatomy and hydraulics in the daisy group: is there a link between insular woodiness and embolism resistance?
2012 Supervisor - Holmer R. - The evolution of lianas in Annonaceae, a wood anatomical and phylogenetic approach
2011 Supervisor - Davin N. - Evolution and development of secondary woodiness in Asteraceae (Senecioneae) and Brassicaceae.
2011 Supervisor - Zwartjes R. - The origin of woodiness within the genus Impatiens.
2010 Supervisor - Eeckhout S. - Evolutie van kruidachtige naar houtige soorten: de zoektocht naar secundair afgeleid hout.
2009 Supervisor - Hamann T. - Bark anatomy of Cornales and Ericales.
2008 Supervisor - Pronk S. - Ecological wood anatomy in Diospyros (Ebenaceae, Ericales).
2006 Supervisor - Pletsers A. - Houtanatomie en pollenmorfologie van Ebenaceae
2003 Supervisor - Van Evelghem L - Houtanatomie en pollenmorfologie van de Marcgraviaceae.

Supervision BSc Students

2014 Supervisor - De Koninck V. - Molecular dating analyses to investigate the possible link between wood formation and drought stress in the Canary Island flora.
2014 Supervisor - van der Meer P. - De rol van houtanatomie in het watertransportsysteem van tomatenplanten.
2013 Supervisor - Schellenberg M. - Wood anatomy of Brassicaceae: secondary woodiness, insular woodiness and differences between insular and continental taxa
2013 Supervisor - Karić D. - Moleculaire datering van eilandhoutigheid op de Canarische Eilanden: een eerste aanzet.
2012 Supervisor - Post Y. - Comparative wood anatomy of island and continental Bassicaceae. Exploring the direction of habit shifts within the family.
2011 Supervisor - van Rongen M. - Vascular cambium formation and secondary growth in Arabidopsis thaliana inflorescence stems
2007 Supervisor - Hamann T. - Houtanatomie van de Icacinaceae s.l.
Available student projects

Public outreach

-The wood symposium of NCB Naturalis (Houtsymposium bij de totstandkoming van ‘s werelds grootste houtcollectie, 22-10-2011) received media attention in national magazines:

 *De Volkskrant, October 21, 2011; Radio Nederland Wereldomroep, October 21, 2011.

-Our Nature paper (Choat et al., 2012) was in the news in more than 10 countries, resulting in more than 50 items in journals, magazines, newspapers, blogs and radio and TV interviews, amongst others:

 *Arbor Vitae 23-2: 20-23. Een droogteperiode brengt bomen snel in moeilijkheden.

-Our Kinabalu – Crocker Range Expedition received much media attention in national and international magazines, websites, radio interviews and TV shows.

-Our Arabidopsis paper (Davin et al 2016) attracted news items for radio 1, radio 538 (live interview on 27-08-2016), and the Nature Today website.

Publications

2017

Journals SCI, peer-reviewed

Trueba S., Pouteau R., Lens F., Field T.S., Isnard S., Olson M.E., Delzon S. 2017. Vulnerability to xylem embolism as a major correlate of the environmental distribution of rain forest species on a tropical island. Plant, Cell & Environment 40: 277-289.
Go to website (DOI)

Cailleret M., Jansen S., Robert E.M.R., DeSoto L., Aakala T., Antos J., Beikircher B., Bigler C., Bugmann H., Caccianiga M., Cada V., Camarero J.J., Cherubini P., Cochard H., Coyea M., Cufar K., Das A., Davi H., Delzon S., Dorman M., Gea-Izquierdo G., Gillner S., Haavik L.J., Hartmann H., Heres A.M., Hultine K., Janda P., Kane J., Kharuk V.I., Kitzberger T., Klein T., Kramer K., Lens F., Levanic T., Linares Calderon C.J.C., Lloret F., Lobo-Do-Vale R., Lombardi F.C., Lopez Rodriguez R., Makinen H., Mayr S., Mészáros I., Metsaranta J.M., Minunno F., Oberhuber W., Ojeda V.S., Papadopoulos A., Peltoniemi M., Petritan A.M., Rohner B., Sangüesa-Barreda G., Sarris D., Smith J.M., Stan A., Sterck F., Stojanovic D., Suarez M.L., Svoboda M., Tognetti R., Torres-Ruiz J., Trotsiuk V., Villalba R., Vodde F., Westwood A., Wyckoff P., Zafirov N., Martínez-Vilalta J. 2017. A global synthesis of radial growth patterns preceding tree mortality. Global Change Biology 23: 1675–1690.
Go to website (DOI)

Neupane S., Lewis P.O., Dessein S., Shanks H., Paudyal S., Lens F. 2017. Evolution of woody life form on tropical mountains in the tribe Spermacoceae (Rubiaceae). American Journal of Botany 104: 419–438.
Go to website (DOI)

Schwallier R., Gravendeel B., de Boer H., van Heuven B.J., Sieder A., Sumail S., van Vugt R., Nylinder S., Lens F. 2017. Evolution of wood anatomical characters in Nepenthes and close relatives of Caryophyllales. Annals of Botany 119: 1179-1193.
Go to website (DOI)

2016

Journals SCI, peer-reviewed

Gleason S.M., Westoby M., Jansen S., Choat B., Hacke U.G., Pratt R.B., Bhaskar R., Brodribb T.J., Bucci S.J., Cao K-F., Cochard H., Delzon S., Domec J-C., Fan Z-X., Field T.S., Jacobsen A.L., Johnson D.M., Lens F., Maherali H., Martínez-Vilalta J., Mayr S., McCulloh K.A., Mencuccini M., Mitchell P.J., Morris H., Nardini A., Pittermann J., Plavcová L., Schreiber S.G., Sperry J.S., Wright I.J., Zanne A.E. 2016. Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytologist 209: 123-136.
Go to website (DOI)

Kidner C., Groover A., Thomas D., Emelianova K., Soliz-Gamboa C., Lens F. 2016. First steps in studying the origins of secondary woodiness in Begonia (Begoniaceae): combining anatomy, phylogenetics, and stem transcriptomics. Biological Journal of the Linnean Society 117: 121-138.
Go to website (DOI)

Li S., Lens F., Espino S., Karimi Z., Klepsch M., Schenk H.J., Schmitt M., Schuldt B., Jansen S. 2016. Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA Journal 37: 152-171.
Go to website (DOI)

Davin N., Edger P.P., Hefer C.A., Mizrachi E., Schuetz M., Smets E., Myburg A.A., Douglas C.J., Schranz M.E., Lens F. 2016. Functional network analysis of genes differentially expressed during xylogenesis in soc1ful woody Arabidopsis plants.. Plant Journal 86: 376-390.
Go to website (URI)

Gleason S.M., Westoby M., Jansen S., Choat B., Brodribb T.J., Cochard H., Delzon S., Hacke U.G., Jacobsen A.L., Johnson D.M., Lens F., Maherali H., Martínez-Vilalta J., Mayr S., McCulloh K.A., Morris H., Nardini A., Plavcová L., Pratt R.B., Schreiber S.G., Zanne A.E. 2016. On research priorities to advance understanding of the safety-efficiency tradeoff in xylem. A response to Bittencourt et al.’s (2016) comment ‘On xylem hydraulic efficiencies, wood space-use and the safety–efficiency tradeoff’: in this issue of New Phytologist, pp. 1152–1155. New Phytologist 211: 1156–1158.
Go to website (DOI)

Lens F., Picon-Cochard C., Delmas C., Signarbieux C., Buttler A., Jansen S., Chauvin T., Chacon Doria L., Arco M. del, Cochard H., Delzon S. 2016. Herbaceous angiosperms are not more vulnerable to drought-induced embolism than angiosperm trees.. Plant Physiology 172: 661-667.
Go to website (DOI)

Lens F., Vos R., Charrier G., Niet T. van der, Merckx V., Baas P., Aguirre Gutierrez J., Jacobs B., Chacon Doria L., Smets E., Delzon S., Janssens S. 2016. Scalariform-to-simple transition in vessel perforation plates triggered by differences in climate during the evolution of Adoxaceae. Annals of Botany 118: 1043-1056.
Go to website (DOI)

Angyalossy V., Pace M.R., Evert R.F., Marcati C.R., Oskolski A.A., Terrazas T., Kotina E., Lens F., Mazzoni-Viveiros S.C., Angeles G., Machado S.R., Crivellaro A., Rao K.S., Junikka L., Nikolaeva N., Baas P. 2016. IAWA List of Microscopic Bark Features. IAWA Journal 37: 517-615.
Go to website (DOI)

2015

Journals SCI, peer-reviewed

Merckx V.S.F.T., Hendriks K.P., Beentjes K.K., Mennes C.B., Becking L.E., Peijnenburg K.T.C.A., Afendy A., Arumugam N., de Boer H., Biun A., Buang M.M., Chen P.-P., Chung A.Y.C., Dow R., Feijen F.A.A., Feijen H., Feijen-van Soest C, Geml J., Geurts R., Gravendeel B., Hovenkamp P., Imbun P., Ipor I., Janssens S.B., Jocqué M. Kappes H., Khoo E., Koomen P., Lens F., Majapun R.J., Morgado L.N., Neupane S., Nieser N., Pereira J.T., Rahman H., Sabran S., Sawang A., Schwallier R.M., Shim P.-S., Smit H., Sol N., Spait M., Stech M., Stokvis F., Sugau J.B., Suleiman M., Sumail S., Thomas D.C., van Tol J., Tuh F.Y.Y., Yahya B.E., Nais J., Repin R., Lakim M. & Schilthuizen M. 2015. Evolution of endemism on a young tropical mountain. Nature 524: 347-350.
Go to website (DOI)

2014

Journals SCI, peer-reviewed

Zhang N.W., Zhao J.J., Lens F., Visser J. de, Menamo T., Fang W., Xiao D., Bucher J., Basnet R.K., Lin K., Cheng F., Wang X.W., Bonnema G. 2014. Morphology, carbohydrate composition and vernalization response in a genetically diverse collection of Asian and European turnips (Brassica rapa subsp. rapa). PLOS ONE 9: e114241.
Go to website (DOI)

2013

Journals SCI, peer-reviewed

Lens F., Tixier A., Cochard H., Sperry J.S., Jansen S., Herbette S. 2013. Embolism resistance as a key mechanism to understand adaptive plant strategies. Current Opinion in Plant Biology 16: 287-292.
Go to website (URI)

Eurlings M.C.M., Lens F., Pakusza C., Peelen T., Wieringa J.J., Gravendeel B. 2013. Forensic identification of Indian Snakeroot (Rauvolfia serpentina Benth. ex Kurz) using DNA barcoding. Journal of Forensic Sciences 58: 822-830.
Go to website (URI)

Lens F., Davin N., Smets E., Arco M. del 2013. Insular woodiness on the Canary Islands: a remarkable case of convergent evolution. International Journal of Plant Sciences 174: 992-1013.
Go to website (URI)

Edited books

Baas P., Battipaglia G., Micco V. De, Lens F., Wheeler E. (eds.). 2013. Wood structure in plant biology and ecology. IAWA Journal 34: 180 p. BRILL, Leiden, The Netherlands. ISBN 9789004265592.

2012

Journals SCI, peer-reviewed

Lens F., Eeckhout S., Zwartjes R., Smets E., Janssens S.B. 2012. The multiple fuzzy origins of woodiness within Balsaminaceae using an integrated approach. Where do we draw the line?. Annals of Botany 109: 783-799.
Go to website (URI)

Lens F., Smets E., Melzer S. 2012. Stem anatomy supports Arabidopsis thaliana as a model for insular woodiness. New Phytologist 193: 12-17.
Go to website (URI)

Appelhans M.S., Heuven B.J. van, Lens F., Baas P. 2012. Phylogenetic and ecological signals in the wood of Spathelioideae (Rutaceae). IAWA Journal 33: 337-353.
Go to website (URI)

Choat B., Jansen S., Brodribb T.J., Cochard H., Delzon S., Bhaskar R., Bucci S.J., Feild T.S., Gleason S.M., Hacke U.G., Jacobsen A.L., Lens F., Maherali H., Martinez-Vilalta J., Mayr S., Mencuccini M., Mitchell P.J., Nardini A., Pittermann J., Pratt R.B., Sperry J.S., Westoby M., Wright I.J., Zanne A.E. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-756.
Go to website (URI)

Lens F., Cooper L., Gandolfo M.A., Groover A., Jaiswal P., Lachenbruch B., Spicer R., Staton M.E., Stevenson D.W., Walls R.L., Wegrzyn J. 2012. An extension of the plant ontology project supporting wood anatomy and development research. IAWA Journal 33: 113-117.
Go to website (URI)

2011

Journals SCI, peer-reviewed

Lens F., Sperry J.S., Christman M.A., Choat B., Rabaey D., Jansen S. 2011. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytologist 190: 709-723.
Go to website (URI)

Kattge J., Diaz S., Lavorel S., Prentice C., Leadley P., Boenisch G., Garnier E., Westoby M., Reich P.B., Wright I.J., Cornelissen J.H.C., Violle C., Harrison S.P., Bodegom P.M. van, Reichstein M., Enquist B.J., Soudzilovskaia N.A., Ackerly D.D., Anand M., Atkin O., Bahn M., Baker T.R., Baldocchi D., Bekker R., Blanco C.C., Blonder B., Bond W.J., Bradstock R., Bunker D.E., Casanoves F., Cavender-Bares J., Chambers J.Q., Chapin F.S. III, Chave J., Coomes D., Cornwell W.K., Craine J.M., Dobrin B.H., Duarte L., Durka W., Elser J., Esser G., Estiarte M., Fagan W.F., Fang J., Fernandez-Mendez F., Fidelis A., Finegan B., Flores O., Ford H., Frank D., Freschet G.T., Fyllas N.M., Gallagher R.V., Green W.A., Gutierrez A.G., Hickler T., Higgins S.I., Hodgson J.G., Jalili A., Jansen S., Joly C.A., Kerkhoff A.J., Kirkup D., Kitajima K., Kleyer M., Klotz S., Knops J.M.H., Kramer K., Kuehn I., Kurokawa H., Laughlin D., Lee T.D., Leishman M., Lens F., Lenz T., Lewis S.L., Lloyd J., Llusia J., Louault F., Ma S., Mahecha M.D., Manning P., Massad T., Medlyn B.E., Messier J., Moles A.T., Mueller S.C., Nadrowski K., Naeem S., Niinemets U., Noellert S., Nueske A., Ogaya R., Oleksyn J., Onipchenko V.G., Onoda Y., Ordonez J., Overbeck G., Ozinga W.A., Patino S., Paula S., Pausas J.G., Penuelas J., Phillips O.L., Pillar V., Poorter H., Poorter L., Poschlod P., Prinzing A., Proulx R., Rammig A., Reinsch S., Reu B., Sack L., Salgado-Negre B., Sardans J., Shiodera S., Shipley B., Siefert A., Sosinski E., Soussana J.-F., Swaine E., Swenson N., Thompson K., Thornton P., Waldram M., Weiher E., White M., White S., Wright S.J., Yguel B., Zaehle S., Zanne A.E., Wirth C. 2011. TRY - a global database of plant traits. Global Change Biology 17: 2905-2935.
Go to website (URI)

Subedi A., Chaudhary R.P., Achterberg C. van, Heijerman Th., Lens F., Dooren T.J.M. van, Gravendeel B. 2011. Pollination and protection against herbivory of Nepalese Coelogyninae (Orchidaceae). American Journal of Botany 98: 1095-1103.
Go to website (URI)

Jansen S., Gortan E., Lens F., Gullo M.A. lo, Salleo S., Scholz A., Stein A., Trifilo P., Nardini A. 2011. Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem?. New Phytologist 189: 218-228.
Go to website (URI)

Hamann T., Smets E., Lens F. 2011. A comparison of paraffin and resin-based techniques used in bark anatomy. Taxon 60: 841-851.
Go to website (URI)

2010

Journals SCI, peer-reviewed

Rabaey D., Lens F., Smets E., Jansen S. 2010. The phylogenetic significance of vestured pits in Boraginaceae. Taxon 59: 510-516.
Go to website (URI)

2009

Journals SCI, peer-reviewed

Lens F., Endress M.E., Baas P., Jansen S., Smets E. 2009. Vessel grouping patterns in subfamilies Apocynoideae and Periplocoideae confirm phylogenetic value of wood structure within Apocynaceae. American Journal of Botany 96: 2168-2183.
Go to website (URI)

Jacobs B., Lens F., Smets E. 2009. Evolution of fruit and seed characters in the Diervilla and Lonicera clades (Caprifoliaceae, Dipsacales). Annals of Botany 104: 253-276.
Go to website (URI)

Lens F., Groeninckx I., Smets E., Dessein S. 2009. Woodiness within the Spermacoceae–Knoxieae alliance (Rubiaceae): retention of the basal woody condition in Rubiaceae or recent innovation?. Annals of Botany 103: 1049-1064.
Go to website (URI)

Chapters in books

Lens F., Jansen S. 2009. Wood and Timber: Theophrastaceae. Series A: Phanerogams 27 Royal Botanical Gardens, Kew, UK.

2008

Journals SCI, peer-reviewed

Lens F., Karehed J., Baas P., Jansen S., Rabaey D., Huysmans S., Hamann T., Smets E. 2008. The wood anatomy of the polyphyletic Icacinaceae s.l., and their relationships within asterids. Taxon 57: 525-552.
Go to website (URI)

Rabaey D., Lens F., Huysmans S., Smets E., Jansen S. 2008. A comparative ultrastructural study of pit membranes with plasmodesmata associated thickenings in four angiosperm species. Protoplasma 233: 255-262.
Go to website (URI)

Melzer S., Lens F., Gennen J., Vanneste S., Rohde A., Beeckman T. 2008. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genetics 40: 1489-1492.
Go to website (URI)

Rabaey D., Huysmans S., Lens F., Smets E., Jansen S. 2008. Micromorphology and systematic distribution of pit membrane thickenings in Oleaceae: tori and pseudo-tori. IAWA Journal 29: 409-424.
Go to website (URI)

Lens F., Endress M.E., Baas P., Jansen S., Smets E. 2008. Wood anatomy of Rauvolfioideae (Apocynaceae): a search for meaningful non-DNA characters at the tribal level. American Journal of Botany 95: 1199-1215.
Go to website (URI)

Jansen S., Pletsers A., Rabaey D., Lens F. 2008. Vestured pits: a diagnostic character in the secondary xylem of Myrtales. Journal of Tropical Forest Science 20: 328-339.
Go to website (URI)

2007

Journals SCI, peer-reviewed

Lens F., Baas P., Jansen S., Smets E. 2007. A search for phylogenetically informative wood characters within Lecythidaceae s.l.. American Journal of Botany 94: 483-502.
Go to website (URI)

Jansen S., Sano Y., Choat B., Rabaey D., Lens F., Dute R.R. 2007. Pit membranes in tracheary elements of Rosaceae and related families: New records of tori and pseudotori. American Journal of Botany 94: 503-514.
Go to website (URI)

Lens F., Schonenberger J., Baas P., Jansen S., Smets E. 2007. The role of wood anatomy in phylogeny reconstruction of Ericales. Cladistics 23: 229-254.
Go to website (URI)

Chapters in books

Baas P., Lens F., Wheeler E.A. 2007. Wood Anatomy. Apocynaceae (subfamilies Rauvolfioideae and Apocynoideae) 1 18: National Herbarium of the Netherlands, Leiden, The Netherlands.

Lens F., Jacobs B., Jansen S., Smets E. 2007. Practicumhandleiding Morfologie en Anatomie. III-94: Uitgeverij ACCO, Leuven, Belgium. ISBN 9789033465208.

Smets E., Lens F. 2007. Cursustekst Fysiologie. III-120: Uitgeverij ACCO, Leuven, Belgium. ISBN 9789033465208.

Smets E., Lens F. 2007. Figuren Morfologie. Uitgeverij ACCO, Leuven, Belgium. ISBN 9789033465208.

Smets E., Lens F. 2007. Cursustekst Morfologie. IV-114: Uitgeverij ACCO, Leuven, Belgium. ISBN 9789033465208.

2006

Journals SCI, peer-reviewed

Rabaey D., Lens F., Smets E., Jansen S. 2006. The micromorphology of pit membranes in tracheary elements of Ericales: New records of tori or pseudo-tori?. Annals of Botany 98: 943-951.
Go to website (URI)

2005

Journals SCI, peer-reviewed

Lens F., Dressler S., Jansen S., Evelghem L. van, Smets E. 2005. Relationships within balsaminoid ericales: A wood anatomical approach. American Journal of Botany 92: 941-953.
Go to website (URI)

Lens F., Jansen S., Caris P., Serlet L., Smets E. 2005. Comparative wood anatomy of the primuloid clade (Ericales s.I.). Systematic Botany 30: 163-183.
Go to website (URI)

Dessein S., Ochoterena H., Block P. de, Lens F., Robbrecht E., Schols P., Smets E., Vinckier S., Huysmans S. 2005. Palynological characters and their phylogenetic signal in Rubiaceae. Botanical Review 71: 354-414.
Go to website (URI)

Janssens S., Lens F., Dressler S., Geuten K., Smets E., Vinckier S. 2005. Palynological variation in balsaminoid Ericales. II. Balsaminaceae, Tetrameristaceae, Pellicieraceae and general conclusions. Annals of Botany 96: 1061-1073.
Go to website (URI)

Lens F., Dressler S., Vinckier S., Janssens S., Dessein S., Evelghem L. Van, Smets E. 2005. Palynological variation in balsaminoid Ericales. I. Marcgraviaceae. Annals of Botany 96: 1047-1060.
Go to website (URI)

2004

Journals SCI, peer-reviewed

Jansen S., Watanabe T., Caris P., Geuten K., Lens F., Pyck N., Smets E. 2004. The distribution and phylogeny of aluminium accumulating plants in the ericales. Plant Biology 6: 498-505.
Go to website (URI)

Jansen S., Choat B., Vinckier S., Lens F., Schols P., Smets E. 2004. Intervascular pit membranes with a torus in the wood of Ulmus (Ulmaceae) and related genera. New Phytologist 163: 51-59.
Go to website (URI)

Lens F., Smets E., Jansen S. 2004. Comparative wood anatomy of Andromedeae s.s., Gaultherieae, Lyonieae and Oxydendreae (Vaccinioideae, Ericaceae s.l.). Botanical Journal of the Linnean Society 144: 161-179.
Go to website (URI)

Lens F., Kron K.A., Luteyn J.L., Smets E., Jansen S. 2004. Comparative wood anatomy of the blueberry tribe (Vaccinieae, Ericaceae s.l). Annals of the Missouri Botanical Garden 91: 566-592.
Go to website (URI)

Lens F., Luteyn J.L., Smets E., Jansen S. 2004. Ecological trends in the wood anatomy of Vaccinioideae (Ericaceae s.l.). Flora: Morphology, Distribution, Functional Ecology of Plants 199: 309-319.
Go to website (URI)

Jansen S., Baas P., Gasson P., Lens F., Smets E. 2004. Variation in xylem structure from tropics to tundra: Evidence from vestured pits. Proceedings of the National Academy of Sciences of the United States of America 101: 8833-8837.
Go to website (URI)

2003

Journals SCI, peer-reviewed

Lens F., Gasson P., Smets E., Jansen S. 2003. Comparative wood anatomy of epacrids (Styphelioideae, Ericaceae s.l). Annals of Botany 91: 835-856.
Go to website (URI)

2001

Journals SCI, peer-reviewed

Jansen S., Lens F., Ntore S., Piesschaert F., Robbrecht E., Smets E. 2001. Contributions to the wood anatomy of the Rubioideae (Rubiaceae). Journal of Plant Research 114: 269-289.
Go to website (URI)

2000

Journals SCI, peer-reviewed

Lens F., Jansen S., Robbrecht E., Smets E. 2000. Wood anatomy of the Vanguerieae (Ixoroideae - Rubiaceae), with special emphasis on some geofrutices. IAWA Journal 21: 443-455.
Go to website (URI)

Lens F., Jansen S., Huysmans S., Robbrecht E., Smets E. 2000. Pollen morphological variation in Vanguerieae (Ixoroideae Rubiaceae). Grana 39: 90-102.
Go to website (URI)