Biere Group

Research in the Biere Group focuses on the ecology and evolution of interactions between plants and their communities of above- and belowground mutualists and antagonists, including mycorrhizae, pollinators, pathogens, insect herbivores and the herbivore’s natural enemies. We aim to understand how such interactions are disrupted or altered by changes in the environment, land use and species introductions, and what the consequences of such alterations are for the functioning, ecology, and evolution of the organisms involved. Such information can help us in the design of management practices in sustainable agriculture and understand and predict how plants respond to environmental change.

Research topics

1. Microbe-induced plant resistance against herbivorous insects.

Many beneficial soil microbes can enhance both plant growth and plant resistance against herbivorous insects. Microbial inoculations are therefore a promising tool to reduce fertilizer and pesticide input in sustainable agriculture and horticulture. We study the impact and mechanisms of microbially-induced resistance against herbivorous insects. We are specifically interested in how the efficacy of such microbially-induced resistance is affected by biotic and abiotic environmental factors in order to understand what is driving the often observed context-dependency of microbially-induced resistance.

Currently we participate in two EU projects on this topic. In MiRA (Microbe-induced resistance to Agricultural Pests, https://mira.ku.dk) we study effects of arbuscular mycorrhizal fungi (AMF) on direct and indirect defense of tomato against insect pests and how that is affected by e.g. light quality and soil fertility (Haymanti Saha, PhD). In EXCALIBUR (Exploiting the multifunctional potential of belowground biodiversity in horticultural farming, https://www.excaliburproject.eu) we study the effects of microbial consortia including AMF and entomopathogenic fungi (EPF) on growth and defense in tomato and strawberry (Shumaila Rasool, PDRA). In a non-model plant species, ribwort plantain (Plantago lanceolata), we use phenotypic and transcriptomics studies to understand how AMF-induced changes in host gene expression and plant traits affect plant responses to herbivory.  

Selected references:  Qu et al. 2021, FiPS (https://doi.org/10.3389/fpls.2021.647372); Lee Díaz et al. 2021, Agronomy (https://doi.org/10.3390/agronomy11071293); Gruden et al. 2020, TiPS (https://doi.org/10.1016/j.tplants.2020.07.008); Ferlian et al. 2018, TiPS (https://doi.org/10.1016/j.tplants.2018.08.008); Biere & Goverse 2016, Annu Rev Pytopathol (https://doi.org/10.1146/annurev-phyto-080615-100245); Wang et al. 2015, J Chem Ecol (https://doi.org/10.1007/s10886-015-0644-0); Biere & Tack 2013, Funct Ecol (https://doi.org/10.1111/1365-2435.12096); Biere & Bennett 2013, Funct Ecol (https://doi.org/10.1111/1365-2435.12100)

tomato greenhouse
Tomato grown with and without beneficial microbes to study effects on pest resistance (MiRA project, Almeria ES)
Tomato fungal bioassay
Bioassay of a fungal pathogen (Botrytis cinerea) in leaves of tomato grown with or without beneficial microbes to enhance resistance.

2. Soil legacy effects on plant growth and resistance

Plant growth alters the composition of the local soil and rhizosphere microbial community through various processes including root exudation. Thus, plants leave a soil “legacy” that can alter the performance of current and future plants growing in such conditioned soils (Plant Soil Feedback, PSF). Likewise, climatic events such as droughts leave their own soil legacies or modify plant-induced legacies. Recently it has become clear that such legacies not only affect future plant growth but also future plant tolerance and resistance to biotic and abiotic stress. We are interested in how such legacies shape plant biotic interactions and how these effects are mediated.

In one of our current projects we investigate how plant growth under fluctuating soil water levels alters soil microbial communities, including AMF, and how these changes affect interactions of subsequently grown plants with nematodes (Hengjun Zhao, PhD).  

Selected references: Heinen et al. 2020, Oikos (https://doi.org/10.1111/oik.06812); Zhu et al. 2018, Oecologia (https://doi.org/10.1007/s00442-018-4245-9)

Mesocosm
Mesocosms to create soil legacies of soil water level and plant growth at NIOO

3. Role of plant secondary metabolites in shaping the plant-associated food web.

Plant secondary metabolites (PSM) often have multiple roles in coping with diverse biotic and abiotic stresses. Variation in the levels of PSM is therefore shaped by highly environment-dependent costs and benefits of their production. Conversely, variation in PSM can be decisive factor in shaping a plant’s biotic environment. We use selection lines of ribwort plantain (Plantago lanceolata), artificially selected  for high and low constitutive levels of a particular class of PSM (iridoid glycosides), as well as induction of these PSM, to study the role of PSM variation in shaping the plant’s interactions with mutualists, pathogens, herbivores and the herbivore’s natural enemies.

Selected references: Rosa et al 2018, Oikos (https://doi.org/10.1111/oik.05437); De Deyn et al. 2009, Oecologia (https://doi.org/10.1007/s00442-009-1312-2); Biere et al. 2004, Oecologia (https://doi.org/10.1007/s00442-004-1603-6); Marak et al. 2003, Evolution (https://doi.org/10.1111/j.0014-3820.2003.tb01496.x); Marak et al. 2000, J Evol Biol (https://doi.org/10.1046/j.1420-9101.2000.00233.x)

Ribwort plantain
Ribwort plantain (Plantago lanceolata) suffering herbivory in the field

4.  Maintenance of mutualisms

The outcome of plant interactions with potentially beneficial organisms such as pollinators and AMF can range from mutualism to antagonism, depending on environmental abiotic and biotic conditions and on the evolution of traits of both partners involved in controlling the interaction. An interesting case are nursery pollinator systems in which insects act both as pollinators and as fruit- or seed-predators. Such systems easily shift from mutualism to antagonism if plants do not have mechanisms to prevent overexploitation (excessive seed predation) by the pollinators. We study the nursery pollinator system of white campion (Silene latifolia) and Hadena moths that have triple roles as pollinators, seed predators and disease vectors. We use studies in natural systems and experimental fields to investigate the role of selective fruit abortion, presence of parasitoid natural enemies of nursery pollinators, plant fungal disease, and environmental conditions in the costs and benefits of the interaction to the partners involved and in the maintenance of the nursery pollinator system. 

Selected references: Boom et al. 2020, Sci Rep (https://doi.org/10.1038/s41598-020-75471-1); Dötterl et al. 2009, J Chem Ecol (https://doi.org/10.1007/s10886-009-9601-0); Biere & Honders, 2006 New Phytol (https://doi.org/10.1111/j.1469-8137.2005.01511.x); Wolfe et al. 2004, Ecol Lett (https://doi.org/10.1111/j.1461-0248.2004.00649.x); Biere et al. 2002, Proc Royal Soc B (https://doi.org/10.1098/rspb.2002.2147)

Silene latifolia experimental field
Experimental population of Silene latifolia at NIOO
Silene latifolia fruits
Fruits infested by larvae of the nursery pollinator Hadena bicruris are preferentially aborted by the plant (left, pedicel incision). Larvae inside fruits are prone to parasitation by Bracon variator (right, using extruding frass from larva as a cue).

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