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Frederic Lens

Dr. F.P. (Frederic) Lens, Senior Researcher - Understanding Evolution

Contact

Email: frederic.lens@naturalis.nl
Phone: 0031 717519320
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never have thought I would become an expert in wood anatomy, a field which I (and many others) initially considered "outdated" and "boring".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 at 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 a 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, secondary woodiness, or derived woodiness. Several hypotheses have tried to explain insular woodiness since Darwin’s original observations, but experimental evidence why plants became woody on islands is scarce at best. I am tackling both main questions applying an ‘eco-evo-devo’ approach, which integrates water flow measures in stems (as a proxy for drought stress resistance) and detailed anatomical observations to investigate structure-function relationships in stems, combined 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).

 

Searching for an interesting project on xylem hydraulics, embedded into an evolutionary framework?

Sylvain Delzon (Univ. Bordeaux, France; sylvain.delzon@u-bordeaux.fr) and Frederic Lens (Naturalis Biodiversity Center, The Netherlands; frederic.lens@naturalis.nl) are looking for a motivated postdoc who wants to apply for a 2y Idex postdoc proposal; deadline around mid November 2018). The postdoc candidate should have at least 3-4 strong publications and will be housed in the Delzon lab (xylem physiology), with several visits to Naturalis (stem anatomy). A good starting point for the proposal text is available, but the candidate is free to adjust the original project according to his/her personal interest. If successful, the position starts between July-December 2019. A tentative title and summary is given below: 

Reaching for the sky: investigating hydraulic failure to understand wood formation in the mustard family (Brassicaceae)
Woody plants (trees and shrubs) cover 30 percent of the planet's land area and offer crucial ecosystem services. It is unclear, however, why some plants are woody and others herbaceous. To this day, scientists have failed to provide satisfying answers, probably because wood formation is a complex process that can be triggered in different and largely understudied ways. One approach to solve this long-standing question is to unveil the key anatomical and physiological stem adaptations that allow herbaceous and woody species to survive in their habitats, through experiments focusing on the dynamics of drought-induced vascular dysfunction (gas embolism formation inside water conducting vessels). The cosmopolitan mustard family (Brassicaceae, 4000 species) serves as an excellent model group to tackle this question. Ten percent of the Brassicaceae species are woody – reaching up to 9m tall – and woodiness has evolved probably more than 100 separate times on both islands and continents. Outcomes of this project will revolutionize our understanding of wood formation, one of the most essential evolutionary innovations on earth. 

 

 

Keywords

wood anatomy, insular woodiness, xylem physiology, molecular wood pathway, derived woodiness, hydraulic failure, drought stress resistance, flowering plants

Current research topics

Is derived woodiness triggered by drought stress? An integrative approach

Assessing why various groups of herbaceous flowering plants have turned back to the ancestrally woody growth form is a complex evolutionary puzzle involving various environmental and abiotic factors, and it may depend on the lineage 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 have recently finished a global derived woodiness database of derived woody species within flowering plants, including nearly 7000 species. 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. Massive levels of embolisms in the water conducting vessels may lead to plant death, meaning that hydraulic failure is one of the most crucial adaptations to drought. I am also interested to investigate which anatomical stem features explain best 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. 

More information: Lens et al 2013ab (Canary Island review, 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 insular woody shrubs (redrawn from Böhle et al 1996).

 

Insular woody daisies (Argyranthemum, Asteraceae) are more resistant to hydraulic failure than their herbaceous relatives

In Doria et al (2018), we found that stems of insular woody daisies (Argyranthemum, Canary Islands) are more resistant to drought-induced hydraulic failure than the stems of their herbaceous counterparts. Thicker intervessel pit membranes in Argyranthemum functionally explain why this insular woody genus is more embolism resistant to drought-induced hydraulic failure, and we also found sound evidence for an indirect link between lignification and resistance to embolism formation (figure). It is tempting to assume that drought has triggered wood formation in the daisy lineage, which agrees with a global ongoing study at the flowering plants revealing that most derived woody shrubs grow in areas with a marked drought period. However, palaeoclimate data for the timeframe in which the insular woody Argyranthemum has originated must first be reconstructed before a causal relationship between drought and increased woodiness can be supported.

https://science.naturalis.nl/media/medialibrary/2018/02/Argyranthemum_overview_1.jpg

Vulnerability curves of the daisy lineage showing that the insular woody species (pink curves) are more resistant to embolism formation than their herbaceous relatives (green curves). The insular woody species have much more lignified stems (c), but more importantly they have thicker intervessel pit membranes (e), which functionally explains the difference in embolism resistance between the woody and herbaceous species (adapted from Doria et al 2018)

 

Additional support for the drought stress hypothesis in Arabidopsis thaliana

We also compared hydraulic failure in a herbaceous stems of wild-type Arabidopsis thaliana plants versus stems of a woody mutant in which two flowering time genes are knocked out (see figure). Again, the woody mutant stems are resistant to hydraulic failure than those of the herbaceous wild-type. 

https://science.naturalis.nl/media/medialibrary/2018/02/Arabidopsis_VC.jpg

Vulnerability curves showing higher xylem vulnerability to embolism in stems of the herbaceous Arabidopsis wild-type compared to stems of the woody mutant (adapted from Lens et al 2013, embolism review).

 

Herbaceous species are not per definition more vulnerable to hydraulic failure than woody species

The water transport pipeline in herbs is assumed to be more vulnerable to drought than in trees due to frequent occurrence of embolisms (gas bubbles) during day time, which might be removed by the occurrence of root pressure over night, especially in grasses. In a recent study (Lens et al 2016), we studied hydraulic failure in herbaceous angiosperms by measuring P50 (pressure inducing 50% loss of hydraulic conductivity) in stems of 26 species - mainly European grasses (Poaceae). Our measurements show a large range in P50 from -0.5 to -7.5MPa (see figure), 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 in these grasses. These resultsshow that both herbs and trees share the ability to withstand hydraulic failure during drought stress.

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

Wide range in P50 values amongst the (mainly herbaceous) species measured in Lens et al (2016). Light green bars indicate grasses (Poaceae), dark green bars represent herbaceous eudicots.

 

Grasses that are more resistant to embolism formation have more lignified stems

Structure-function correlations in our grass dataset reveal that the more resistant species are more lignified (figure). 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).

  

Unravelling the molecular wood pathway leading to insular woodiness

We have performed transcriptome experiments in Arabidopsis thaliana using RNA-seq of different stem developmental stages that are important to wood formation, i.e. herbaceous stage, cambium stage and wood stage (Davin et al 2016). This first transcriptome dataset will provide the basis for future planned studies that want to infer whether transitions towards derived woodiness in independent lineages 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 Davin et al (2016) paper, we did not found evidence for the presence of only one 'master gene' that would turn on the wood pathway in the woody Arabidopsis mutant. Instead, most of the hundreds of genes differentially expressed between crucial stem developmental stages were closely linked into a dense gene network (figure). We interpreted this gene network as an alternative mechanism to explain the apparent simple genetic trigger causing rampant evolutionary transitions towards derived 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 the hundreds of independent life form transitions.

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

      https://science.naturalis.nl/media/medialibrary/2018/02/Arabidopsis_network_clean_fig_1.jpg
 

Is there a common genetic mechanism leading to derived woodiness in various angiosperm groups with different woody life forms and habitats (above)? Interaction network of genes differentlally expressed between the cambium stage and the wood stem stage in the Arabidopsis mutant (below) may indicate that several regulatory genes embedded into a shared gene interaction network - rather than a single master gene - could be responsible for the hundreds of independent transitions towards derived woodiness (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.

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.

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

Jahanbanifard M. Identification of ebony woods used in music instruments based on computational phenotyping and chemical profiling 

Thonglim A.

Teaching

Courses

Since 2010 I am involved in the courses Biodiversity of Plants - Tree of Life (part plant anatomy; 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

2018 Supervisor - Hooft van Huysduynen A. - A molecular dating approach for evaluation of the link between palaeo-drought events and insular woodiness in several Canary Island lineages
2017 Co-supervisor - Liang C. - Wood species recognition using convolutional neural networks
2017 Supervisor - Xu H. - Investigating stem anatomical characters amongst 12 populations of the grass Dactylis glomerata L. across Europe
2017 Supervisor - Adamo I. - Investigating convergent evolutionary shifts towards derived woodiness within the Brassicaceae tribes Anastaticeae and Erysimeae:
 a molecular phylogenetic approach
2017 Supervisor - Li K. - Investigation of habit transitions towards derived woodiness in the Brassicaceae tribes Alysseae, Iberideae, Lepidieae and Thelypodieae
2017 Supervisor - Meijs C. - Embolism resistance and stem anatomy of herbaceous Brassicaceae on the island of Tenerife (Canary Islands)
2015 Supervisor - Zaini N.H. - Stem anatomy and growth habit evolution of Asian Begonia (Begoniaceae)
2015 Co-supervisor - 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

2018 Supervisor - Karabayir B. - Duidt het paleoklimaat op de Canarische Eilanden op een mogelijke link tussen houtvorming en droogtestress? Een benadering via moleculaire stamboomdatering.
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

2018

Journals SCI, peer-reviewed

Pfautsch S., Aspinwall M.J., Drake J.E., Chacon Dória L., Langelaan R.J.A., Tissue D.T., Tjoelker M.G., Lens F. 2018. Traits and trade-offs in whole-tree hydraulic architecture along the vertical axis of Eucalyptus grandis. Annals of Botany 121: 129-141.
Go to website (DOI)

Ahmad H.B., Lens F., Capdeville G., Burlett R., Lamarque L.J., Delzon S. 2018. Intraspecific variation in embolism resistance and stem anatomy across four sunflower (Helianthus annuus L.) accessions. Physiologia Plantarum 163: 59-72.
Go to website (DOI)

Doria L.C., Podadera D.S., del Arco M., Chauvin T., Smets E., Delzon S., Lens F. 2018. Insular woody daisies (Argyranthemum, Asteraceae) are more resistant to drought-induced hydraulic failure than their herbaceous relatives. Functional Ecology 32: 1467-1478.
Go to website (DOI)

Volaire F., Lens F., Cochard H., Xu H., Chacon-Doria L., Bristiel P., Balachowski J., Rowe N., Violle C., Picon-Cochard C. 2018. Embolism and mechanical resistances play a key role in dehydration tolerance of a perennial grass Dactylis glomerata L.. Annals of Botany: 1-12.
Go to website (DOI)

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.
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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.
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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.
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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.
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Hamann T., Smets E., Lens F. 2011. A comparison of paraffin and resin-based techniques used in bark anatomy. Taxon 60: 841-851.
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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.
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2009

Journals SCI, peer-reviewed

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