Research Theme

Variation in plant developmental programs:
Ecological implication & micro-evolutionary dynamics

Plant form and function, growth and ontogeny, as well as a plant life histories are expressions of developmental programs, which act as central control and coordinating mechanisms in the dynamic interaction between plants and their environments. Due to the modular construction of plants, developmental programs include only a few processes at the organizational levels of meristems, such as allocation of meristems to different faits (flowering, vegetative branching, dormancy) and cell differentiation. Nevertheless they form the functional basis for a wide array of plant traits, ranging form plant architecture to dynamic life cycle characteristics such as the timing of life history events and the duration of life stages, thereby determining the spatio-temporal configuration of growth and development.

Research Interest

I am mainly interested in the genetic basis of variation in developmental programs and the fitness consequences of such variation. My research aims at

(a) elucidating the ecological role of specific developmental programs in shaping plant responses to environmental conditions,

(b) quantifying genetic and plastic variation in developmental programs along environmental gradients, and

(c) investigating how genetic variation and phenotypic flexibility in developmental programs translate into fitness differences in natural environments. I am doing this by comparing wide arrays of genotypes of plants expressing phenotypic variation under greenhouse and field conditions

Evolution and consequences of genetic and phenotypic variation in functional plant traits

Small changes in developmental programs can explain large variation in plant architecture, resulting in considerable fitness differences among genotypes subjected to similar environmental conditions. Difference among developmental programs can be constitutive or plastic. Constitutive differences result in the expression of different phenotypes under the same environmental conditions while plastic responses to the environment result in the expression of different phenotypes of the same genotype induced by different environmental conditions. Evolution of specific values for constitutive and plastic traits depends on the temporal and spatial variation of environmental characteristics experienced in natural habitats and the costs and benefits associated to the expression of specific trait values. The clonal herb Trifolium repens is one of the species expressing an up to 4-fold within population constitutive variation in trait expression. The potential to plastically elongate the petioles in response to shading, however, is independent of the petiole length expressed under high light conditions (Weijschede et al. 2006). The specific costs and benefits associated to both, constitutive and plastic variation in spacer length, differs among experimental treatments (Weijschede et al. 2006, 2008b), supporting the notion that the direction and magnitude of selection on trait expression can differ among different micro-environments. These data, however, do not show in howfar constitutive and plastic trait variation will actually be selected for in natural environments. In future my research will aim at quantifying the frequency and spatio-temporal patterns of selection pressures affecting micro-evolutionary trait changes and the generation of trait variation under field conditions. This will contribute to our understanding of the pathways and outcomes of selection and micro-evolution in natural populations.

Ecology and evolution of adaptive phenotypic plasticity

If plants are subjected to low light conditions they generally elongate their vertical structures (stems or petioles), thereby increasing light interception. Selection for such plastic responses depends on the balance between costs and benefits associated with plastic changes of the phenotypes, but also on the frequency of environments selecting for expression of specific phenotypes. Comparative experiments on closely related species in which different developmental programs lead to the expression of constitutively different growth forms (i.e. plants with horizontal and vertical stems) have shown that different structures respond differently to shading. While in plants with a predominantly erect growth form mainly internodes elongate under shaded conditions, it is the petioles which elongate under shaded conditions in clonal plants (Huber 1996; Huber et al. 1998). This indicates that different - growth-form-specific - selection pressures act on phylogenetically homologous structures and that closely related species have evolved conspicuously different response patterns. These selection pressures favouring the elongation of vertical spacers appear to be strong enough to results in a relatively fast changes on the strength of plastic elongation plants can express. The strength of selective forces affecting the evolution of plasticity depends on the frequency and strength of selection on alternative phenotypes within populations. Experiments on Impatiens capensis have revealed that within a natural population different phenotypes are favoured on a relatively small scale. It can be concluded that if within the same population micro-environmental variation in environmental conditions exist that favour different phenotypes within the dispersal radius of a plant across generations, plasticity will be selected for (Huber et al. 2004; von Wettberg et al 2005).

Mechanisms determining spacer length

The size of plant structures can be determined by either cell elongation or cell division. Newly formed cells that no longer participate in the division process differentiate into their destined function and elongate until they reach their mature sizes. Both, cell division and cell elongation are distinctly different developmental processes which are separated in time and different genes are independently involved in the processes regulating cell proliferation and cell elongation. Increase in size can thus achieved by either producing more cells or larger cells. 

Both, past and present selection affect the relative contribution of these two developmental processes to organ size variation, as the number and size of cells and their response to environmental conditions differs in genotypes originating from different habitats. Within habitat constitutive variation in organ size is mainly achieved by the production of more cells. Shade induced plastic elongation is by achieved by both, increase in cell size and cell number. There is a negative genetic correlation in the main mechanisms used to produce longer organs (Weijschede et al. 2008a).

As cell division involves additional investment into cell material producing larger organs by means of cell elongation may be more costly in terms of biomass compared to spacer elongation by means of cell elongation. On the other hand tissue made of more but smaller cells might have a higher density of cell walls providing rigidity and strength, and thus be more resistant to buckling or rupture. My ongoing research deals with the short and long term consequences associated to the expression of different developmental processes contributing to organ size variation (Huber et al 2008; Wijschede et al. 2008a).

Evolutionary ecology of clonal plants

Many species are characterized by horizontal growth of their stems and the ability to form potentially independent, but genetically identical offspring along the stems. Switching from vertical (unitary) to horizontal (clonal) growth has dramatic effects on several features of the plants, including the mechanisms plants have evolved to cope with light limitation (see previous section) to the genetic composition of populations.

Clonal herbs such as Trifolium repens are characterized by simple modular structure. Each module basically consists of an internode, one leaf, one axillary meristem and roots. This is the smallest potentially independent unit of the plants. In clonal species selection can act on different levels of plant organization, ranging from of the individual ramet (module), interconnected groups of ramets to all plants sharing the same genetic information. Depending on the type of process, selection may predominantly act on one or more of the hierarchical level (de Kroon et al 2005). Evolutionary responses, however, will be expressed on the highest level.

In clonal herbs such as Trifolium repens each axillary meristem can display basically 3 different fates. It may stay dormant, produce a new vegetative shoot or produce a flower. A meristematic trade-off between these three function is inherent to the growth of Trifolium repens. The decision of which function the meristems are allocated to can have significant effects on future growth of these plants (Huber & During 2001). I study how genetic variation of the meristematic allocation patterns is translated in to future performance differences and whether plants can change meristematic allocation patterns in response to their immediate environment). Furthermore I am interested in the mechanisms underlying the switch of meristem allocation to different functions and the genetic basis thereof.

PhD-students

• Jelmer Weijschede (2002-2007): On the variation of a functional trait: Mechanisms and consequences of petiole length variation in Trifolium repens.
• Xin Chen (2005-2009): Variation in submergence induced shoot elongation in Rumex palustris.

Curriculum vitae

2003 - now	Assistant Professor, Radboud University Nijmegen, The Netherlands	.
2000 - 2002	Post-doc, Brown University, Providence, RI, USA	advisor: Prof. Johanna Schmitt
1998-1999	Coordinator of Dutch-Russian Scientific Collaboration, Utrecht University, The Netherlands	.
1997	Post-doc, Institute for Low Temperature Science, Hokkaido University, Sapporo, Japan	advisor: Dr. Jun-Ichirou Suzuki
1997	PhD, Utrecht University, The Netherlands	advisors: Prof. Dr. Marinus Werger Dr. Heinjo During
1993	MSc (Magister rerum naturae) Paris Lodron University Salzburg, Austria	advisor: A.o.Prof. Doz. Dr.Paul Heiselmayer

Collaborators over the years

Niels Anten	Utrecht University, The Netherlands)
Ariel Novoplansky	Blaustein Institutes of Desert Research, Sde Broker, Israel
Luis Santamaria	University of the Balearic, IMEDEA, Mallorca, Spain
Maxine Watson	University of Indiana, Bloomington, IN, USA
Eric von Wettberg	University ov California at Davis, CA, USA
Dennis F. Whigham	Smithonian Environmental Research Center, MD, USA

Publications by Heidrun Huber

• Jongejans E, Huber H & de Kroon H (2010) Scaling up phenotypic plasticity with hierarchical population models. Evolutionary Ecology in press PDF

• Chen X, Huber H, de Kroon H, Peeters AJM, Poorter H, Voesenek LACJ & Visser EJW (2009) Intraspecific variation in the magnitude and pattern of flooding-induced shoot elongation in Rumex palustris. Annals of Botany 104:1057–1067 PDF

• Anten NPR, von Wettberg EJ, Pawlowski M & Huber H (2009) Interactive effects of spectral shading and mechanical stress on the expression and costs of shade avoidance. American Naturalist 173:241-255 PDF

• de Kroon H, Visser EJW, Huber H, Mommer L & Hutchings MJ (2009) A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant, Cell and Environment 32:704-712 PDF

• Huber H, Jacobs E & Visser EJW (2009). Variation in flooding-induced morphological traits in natural populations of white clover (Trifolium repens L.) and their effects on plant performance during soil flooding. Annals of Botany 103:377-386 PDF

• Weijschedé J, Berentsen R, de Kroon H & Huber H (2008) Variation in petiole and internode length affects plant performance in Trifolium repens under opposing selection regimes. Evolutionary Ecology 22:383–397 PDF

• Weijschedé J, Antonise K, de Caluwe H, de Kroon H & Huber H (2008) The effects of cell number and cell size on petiole length variation in a stoloniferous herb. American Journal of Botany 95:41–49 PDF

• Huber H, de Brouwer J, de Caluwe H, Wijschedé J & Anten NPR (2008) Shade induced changes in biomechanical petiole properties in the stoloniferous herb Trifolium repens. Evolutionary Ecology 22:399–416 PDF

• Weijschedé J, Martínková J, de Kroon H & Huber H (2006) Shade avoidance in Trifolium repens: costs and benefits of plasticity in petiole length and leaf size. New Phytologist 172:655–666 PDF

• Mommer L, Lenssen JPM, Huber H, Visser EJW & de Kroon H (2006) Ecophysiological determinants of plant performance under flooding: a comparative study of seven plant families. Journal of Ecology 94:1117–1129 PDF

• Werger MJA & Huber H (2006) Tuber size variation and organ preformation constrain growth responses of a spring geophyte. Oecologia147:396–405 PDF

• von Wettberg EJ, Huber H & Schmitt J (2005) Interacting effects of microsite quality, plasticity, and dispersal distance from the parental site on fitness in a natural population of Impatiens capensis. Evolutionary Ecology Research 7:531-548 PDF

• de Kroon H, Huber H, Stuefer JF & van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytologist 166: 73-82 PDF

• Huber H, Whigham DF & O'Neill J (2004) Timing of disturbance changes the balance between growth and survival of parent and offspring ramets in the clonal forest understory herb Uvularia perfoliata. Evolutionary Ecology 18:521-539 PDF

• Huber H, Kane NC, Heschel MS, von Wettberg EJ, Banta J, Leuck AM & Schmitt J (2004) Frequency and microenvironmental pattern of selection on plastic shade-avoidance traits in a natural population of Impatiens capensis. American Naturalist 163:584-563 PDF

• Schmitt J, Stinchcombe JR, Heschel MS & Huber H (2003) The adaptive evolution of plasticity: phyto-chrome-mediated shade avoidance responses. Integrative and Comparative Biology 43:459–469 PDF

• Stuefer JF, Erschbamer B, Huber H & Suzuki JI (2002) The ecology and evolutionary biology of clonal plants: An introduction to the proceedings of Clone-2000. Evolutionary Ecology 15:223-230 PDF

• Huber H & During HJ (2001) No long-term costs of meristem allocation to flowering in stoloniferous Trifolium species. Evolutionary Ecology 14:731-748 PDF

• Stuefer JF & Huber H (1999) The role of stolon internodes for ramet survival after clone fragmentation in Potentilla anserina. Ecology Letters 2:135-139 PDF

• Huber H, Lukács S & Watson MA (1999) Spatial structure of stoloniferous herbs: an interplay between architectural blue-print, ontogeny and phenotypic plasticity. Plant Ecology 141:107-115  PDF

• Stuefer JF & Huber H (1998) Differential effects of light quantity and spectral light quality on growth, morphology and development in two stoloniferous Potentilla species. Oecologia 117:1-8 PDF

• Huber H, Fijan A & During HJ (1998) A comparative study of spacer plasticity in erect and stoloniferous herbs. Oikos 81:576-586 PDF

• Huber H & Hutchings MJ (1997) Differential response to shading in orthotropic and plagiotropic shoots of the clonal herb Glechoma hirsuta. Oecologia 112:485-491 PDF

• Huber H & Wiggerman L (1997) Shade avoidance in the clonal herb Trifolium fragiferum: a field study with experimentally manipulated vegetation height. Plant Ecology 130:53-62 PDF

• Huber H & Stuefer JF (1997) Shade-induced changes in the branching patterns of a stoloniferous herb: functional response or allometric effect? Oecologia 110:478-486 PDF

• Huber H, Stuefer JF & Willems JH (1996) Environmentally induced carry-over effects on seed production, germination and seedling performance in Bunium bulbocastanum (Apiaceae). Flora 191:353-361

• Huber H (1996) Plasticity of internodes and petioles in prostrate and erect Potentilla species. Functional Ecology 10:401-409 PDF

• Huber H (1995) Growth form and plasticity of the hybrid Potentilla anglica and its two parent species. Abstracta Botanica 19:61-73

PhD Thesis

Huber H (1997) Architectural plasticity of stoloniferous and erect herbs in response to light climate. Utrecht University