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Exploring the co-operativity of secretory structures for defense and pollination in flowering plants

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Abstract

Main conclusion

In flowers multiple secretory systems cooperate to deliver specialized metabolites to support specific roles in defence and pollination. The collective roles of cell types, enzymes, and transporters are discussed.

Abstract

The interplay between reproductive strategies and defense mechanisms in flowering plants has long been recognized, with trade-offs between investment in defense and reproduction predicted. Glandular trichomes and secretory cavities or ducts, which are epidermal and internal structures, play a pivotal role in the secretion, accumulation, and transport of specialized secondary metabolites, and contribute significantly to defense and pollination. Recent investigations have revealed an intricate connection between these two structures, whereby specialized volatile and non-volatile metabolites are exchanged, collectively shaping their respective ecological functions. However, a comprehensive understanding of this profound integration remains largely elusive. In this review, we explore the secretory systems and associated secondary metabolism primarily in Asteraceous species to propose potential shared mechanisms facilitating the directional translocation of these metabolites to diverse destinations. We summarize recent advances in our understanding of the cooperativity between epidermal and internal secretory structures in the biosynthesis, secretion, accumulation, and emission of terpenes, providing specific well-documented examples from pyrethrum (Tanacetum cinerariifolium). Pyrethrum is renowned for its natural pyrethrin insecticides, which accumulate in the flower head, and more recently, for emitting an aphid alarm pheromone. These examples highlight the diverse specializations of secondary metabolism in pyrethrum and raise intriguing questions regarding the regulation of production and translocation of these compounds within and between its various epidermal and internal secretory systems, spanning multiple tissues, to serve distinct ecological purposes. By discussing the cooperative nature of secretory structures in flowering plants, this review sheds light on the intricate mechanisms underlying the ecological roles of terpenes in defense and pollination.

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Data availability

The datasets generated or analysed during this study are available from the corresponding author on reasonable request.

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Funding

This work was financially supported in China by the China Post­doctoral Science Foundation (2019M662679 and 2018M640720), the National Key Research and Development Project (2019YFD1001500), National Natural Science Foundation of China (31902051) and the fundamental Research Funds for the Central Universities (2662019FW016).

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Authors and Affiliations

  1. National Key Laboratory for Germplasm Innovation, Unifilization of Horticultural Crops Huazhong Agricultural University, Wuhan, 430070, China

    Jinjin Li, Hao Hu, Hansen Fu, Tuo Zeng, Jiawen Li & Caiyun Wang

  2. Guangdong Provincial Key Lab of Ornamental Plant Germplasm Innovation and Utilization, Environmental Horticulture Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China

    Jie Li

  3. Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Manqun Wang

  4. Business Unit Bioscience, Wageningen Plant Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands

    Maarten A. Jongsma

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  1. Jinjin Li
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  2. Hao Hu
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  3. Hansen Fu
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  4. Jie Li
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  5. Tuo Zeng
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  6. Jiawen Li
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  7. Manqun Wang
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  8. Maarten A. Jongsma
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  9. Caiyun Wang
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Contributions

JJL wrote the initial draft; JJL, HSF and JL performed the experiments and drew the figures; HH, MQW, TZ, JWL, MJ and CYW revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Maarten A. Jongsma or Caiyun Wang.

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Communicated by Gerhard Leubner.

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Li, J., Hu, H., Fu, H. et al. Exploring the co-operativity of secretory structures for defense and pollination in flowering plants. Planta 259, 41 (2024). https://doi.org/10.1007/s00425-023-04322-w

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