How a botanical textbook from 17 years ago helped ecologists deepen their understanding of nature

In general, since the book is based on the decades of teaching practice experienced by the author, we can feel a sense of lightness and simplicity in the lines of the words, highlighting the profound academic skills and extensive knowledge of the author.

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Figure 1. The cover of Plant Developmental Biology.

I happened to discover a botanical textbook named, “Plant Development Biology” that was published 17 years ago, by chance (Figure 1) (1). After a rough skim through its catalog, I decided to purchase it, and then, I read it intensively. As expected, the book brought me beauty in words, but most importantly, it deepened my understanding of some current ecological issues. For example, the author, Professor Bai Shu-Nong, clearly defined the concept of the processes of plant development, believing that the flower is the continuation of a branch; this helps understand the concept of litter in ecological research. Moreover, the conceptual explanation of the "epigenetic effect" helped me understand ecological phenomena such as "ecological memory" and "legacy effect."

Although the book has less than 200 pages, it is extremely rich in content. As mentioned earlier, the first attractive thing is its catalog, which is divided into a total of eight chapters. In addition to the introduction of the first chapter, the discussion gradually progresses from the plant life cycle to the core processes of plant development. The focus of the book is the discussion on lateral organs, while the core part is the formation and development of floral organs. In my opinion, the most distinctive feature of each chapter is the clear definition of concepts related to plant development, which is of great help in understanding the process of plant development. In general, since the book is based on the decades of teaching practice experienced by the author, we can feel a sense of lightness and simplicity in the lines of the words, highlighting the profound academic skills and extensive knowledge of the author. For instance, when discussing the leaf morphology, the author stated that "the size of the vegetative leaf can range from less than 1 mm of the leaflet of Wolffia arrhiza to the diameter of the lotus leaf greater than 1 m or the length of the palm leaf more than 2 m; it can also range from whole round to coniferous needles; even for the same plant, the vegetative leaves of different parts or during different developmental stages have different shapes, such as heteromorphic leaves." The book contains numerous elaborative observations.

In shaping the diverse landscapes of the earth, flowering plants are essential components, bearing as many as 370,000 species (2). This is precisely because, for centuries, the love for flowers has inspired generations of botanists to conduct in-depth research on plant development. In recent years, meaningful progress has been made in flower morphology (color and structure), scent, and relationships between flowers and pollinating insects (311). For a person engaged in ecological research, the inspiring point of the book reads that "flowers are metamorphosed branches, and flower organs are metamorphosed leaves." Indeed, considering flowers as metamorphosed branches, it is easier to understand why ecologists sometimes combine flowers and leaves as a compound indicator when collecting litter in forests. Litter is a general term for fallen plant organs that includes the leaves, flowers, fruits, branches, among others. It is a key component for reabsorption and utilization of nutrients in the forest; it is also of great significance in the study of the global carbon cycle and climate change.

Regarding floral organs as metamorphic leaves makes it easier to understand a plant physiology phenomenon, that is, why botanists like to compare the stomata on petals with the stomata on leaves. Although biologists have limited knowledge about the biological meaning of the stomata in floral organs (mainly sepals and petals) (12), by comparing the stomata in floral organs and leaves to environmental factors such as vapor pressure deficit (VPD), scientists discovered some interesting phenomena, such as the confirmation that stomatal transpiration in floral organs is more sensitive to VPD than that in leaves (13). Flowers being the major organs to ensure the success of reproduction, compared with leaves, are better in water content retention, homeostasis, and anti-cavitation embolism (14); the underlying mechanism includes direct access of water from the nearby stem and the production of extracellular polysaccharides (13, 15). A vivid case that illustrates the homology of leaves and petals is the Chinese endemic plant Davidia involucrata; because of the pair of white heart-shaped bracts found outside the inflorescence of Davidia involucrata, it is called "dove tree," and the bracts are supposed to have evolved from the leaves (Figure 2) (16).

Figure 2. The flowers of Davidia involucrata. Credit: Xu Ye-Chun.

In recent years, a principal focus in ecological research is how plants respond to biotic (such as insect herbivores) and abiotic (such as drought) stresses and plants ability to cope with stress till the next generation (1719). Compared to animals that can move, plants are affected by adverse external conditions and can sometimes exhibit tolerance. This aspect shaped the different plant morphologies and vegetation patterns we have observed and suggested how the adaptability of plants to the external environment has been inherited from generation to generation. Several recent studies have shown (20, 21) that plant progenies can inherit the ability to cope with drought and other stresses. Differences in the genomic sequence of the parent and offspring may be nonexistent; however, the factor responsible for such a "memory" is the "epigenetic effect" that the book emphasized. The factor commonly called "epigenetic effect" refers to the gene expression caused by a change in the chromatin spatial structure of plants (including DNA and histones); however, this does not affect the sequence but can be transmitted between cells through mitosis. Scientists currently have the knowledge that DNA methylation is one of the main modes of transmission. In the 7th International Horticulture Research Conference held July 2, the report "Plant Epigenetics and Molecular Breeding" by plant biologist Zhu Jian-Kang mainly discussed DNA methylation in recent years. Zhu also quoted a human development case titled "Why Your DNA Isn't Your Destiny" to explain the effect of DNA methylation on human traits. In the botanical textbook, the author also repeatedly mentioned the role of the "epigenetic effect" in plant development (P83; P86; P122; P150), showing that this concept helps greatly in understanding the nature of life sciences. Visualize two forests, A and B (Figure 3), the trees of forest A are often subjected to droughts, while forest B is exposed to a mesic environment. When the next drought occurs, forest A and its surrounding floor vegetation would probably cope better with the drought due to drought stresses experienced overtime (memory). In this situation, we can imagine how much methylation and demethylation of plants may have occurred in the forests! When we observe natural phenomena with multidisciplinary knowledge, we can aspire to be like Humboldt and Darwin (22), "both the telescopic and microscopic modes of thinking, that is, seeing the landscapes and all its slenderness." is definitely, no easy task.

Figure 3. Coniferous forests in autumn. Credit: Serguei Fomine.

An interesting discussion in the book is the ridicule of "mechanism research." Indeed, in early plant biology research, measuring the morphological, physiological, and biochemical indicators (such as the length of cells, respiration, and enzyme activity) after applying plant hormones was considered "mechanism research." Although there are historical reasons for this consideration, I think the most important reason may be the scale of mechanism research. The common word "mechanism" is generally a reasonable description of the principles behind natural phenomena. Mechanism research has obvious "top-down" characteristics; for example, for geography and geology researches, an ecological study can become a mutual mechanism; and variable analysis in plant ecophysiology can be the mechanism of ecological research; however, understanding the plant development phenomena that we observe requires measurements and researches at the molecular, biochemical, and cellular levels.

The book certainly needs an improved present version to accommodate more information. For example, when discussing the influence of environmental factors on plant morphogenesis, the book contains only a description of the influence of light, having less discussion on temperature (thermomorphogenesis). Botanists and ecologists have observed many temperature effects on morphogenesis, one of which is, increased radiation or rise in temperature may cause leaf thickness. There is no mention of the current popular gene-editing technology and systems (such as CRISPR-Cas9), which have become powerful techniques in studying the biology of plant development (23). Zachary Lippman and his colleagues in the Cold Spring Harbor Laboratory used these techniques to achieve fascinating results in the development of flowers. The scientists used gene-editing techniques to create a slight mutation in the SP5G gene, a gene encoding anti-florigen, making tomatoes less sensitive to the duration of sunlight, and hastening flowering to two weeks in advance (24). This result is related to the fact that this technology was only applied to the study of plant development in 2016.

Regardless of the change in research objectives and methods, for a person engaged in ecological study, the book Plant Developmental Biology provides elaborate process and mechanism explanations, which deepens our understanding of ecology and the principles behind nature. With the accumulation of empirical research in the field of plant developmental biology (2528), this ancient discipline/book will presumably continue to help ecologists understand basic ecological concepts.

References

  1. S.-N. Bai, Plant Developmental Biology (Peking University Press, Beijing, 1st Editio., 2003).
  2. E. N. LUGHADHA et al., Counting counts: revised estimates of numbers of accepted species of flowering plants, seed plants, vascular plants and land plants with a review of other recent estimates. Phytotaxa. 272, 82 (2016).
  3. E. Reyes, H. Sauquet, S. Nadot, Perianth symmetry changed at least 199 times in angiosperm evolution. Taxon. 65, 945–964 (2016).
  4. T. N. C. Vasconcelos et al., Floral uniformity through evolutionary time in a species-rich tree lineage. New Phytol. 221, 1597–1608 (2019).
  5. J. Ng, S. D. Smith, Widespread flower color convergence in Solanaceae via alternate biochemical pathways. New Phytol. 209, 407–417 (2016).
  6. H. Sauquet et al., The ancestral flower of angiosperms and its early diversification. Nat. Commun. 8 (2017), doi:10.1038/ncomms16047.
  7. P. Vaidya et al., Ecological causes and consequences of flower color polymorphism in a self-pollinating plant (Boechera stricta). New Phytol. 218, 380–392 (2018).
  8. E. Moyroud et al., Disorder in convergent floral nanostructures enhances signalling to bees. Nature. 550, 469–474 (2017).
  9. C. Minnaar, B. Anderson, M. L. de Jager, J. D. Karron, Plant–pollinator interactions along the pathway to paternity. Ann. Bot. 123, 225–245 (2019).
  10. H. S. Ishii, M. X. Kubota, S. G. Tsujimoto, G. Kudo, Association between community assemblage of flower colours and pollinator fauna: a comparison between Japanese and New Zealand alpine plant communities. Ann. Bot. 123, 533–541 (2019).
  11. A. L. Parachnowitsch, J. S. Manson, N. Sletvold, Evolutionary ecology of nectar. Ann. Bot. 123, 247–261 (2019).
  12. F. Zhang, M. R. C. Murphy, T. J. Brodribb, A. A. Cardoso, G. J. Jordan, Similar geometric rules govern the distribution of veins and stomata in petals, sepals and leaves. New Phytol. 219, 1124–1234 (2018).
  13. A. B. Roddy, T. E. Dawson, K. A. Simonin, K. A. Mcculloh, C. R. Brodersen, Water relations of Calycanthus flowers: Hydraulic conductance, capacitance, and embolism resistance. Plant. Cell Environ. 41, 2250–2262 (2018).
  14. A. B. Roddy, G. Jiang, K. Cao, K. A. Simonin, C. R. Brodersen, Hydraulic traits are more diverse in flowers than in leaves. New Phytol. 223, 193–203 (2019).
  15. S. M. CHAPOTIN, N. M. HOLBROOK, S. R. MORSE, M. V. GUTIERREZ, Water relations of tropical dry forest flowers: pathways for water entry and the role of extracellular polysaccharides. Plant, Cell Environ. 26, 623–630 (2003).
  16. J. Sun, Y. Gong, S. S. Renner, S. Huang, Multifunctional Bracts in the Dove Tree Davidia involucrata (Nyssaceae: Cornales): Rain Protection and Pollinator Attraction. Am. Nat. 171, 119–124 (2008).
  17. E. Fleta-Soriano, S. Munné-Bosch, Stress Memory and the Inevitable Effects of Drought: A Physiological Perspective. Front. Plant Sci. 7 (2016), doi:10.3389/fpls.2016.00143.
  18. J. A. Lau, J. T. Lennon, Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl. Acad. Sci. 109, 14058–14062 (2012).
  19. Ł. Wojtyla, E. Paluch-Lubawa, E. Sobieszczuk-Nowicka, M. Garnczarska, in Priming-Mediated Stress and Cross-Stress Tolerance in Crop Plants (Elsevier, 2020; https://linkinghub.elsevier.com/retrieve/pii/B9780128178928000076), pp. 115–131.
  20. C. Forestan et al., Epigenetic signatures of stress adaptation and flowering regulation in response to extended drought and recovery in Zea mays. Plant. Cell Environ. 43, 55–75 (2020).
  21. V. P. Bulgakov, H.-C. Wu, T.-L. Jinn, Coordination of ABA and Chaperone Signaling in Plant Stress Responses. Trends Plant Sci. 24, 636–651 (2019).
  22. A. Wulf, The invention of nature: The adventures of Alexander von Humboldt, the lost hero of science (John Murray, London, UK, 2015).
  23. P. Bhalothia, K. Yajnik, A. Alok, S. K. Upadhyay, in Genome Engineering via CRISPR-Cas9 System (Elsevier, 2020; https://linkinghub.elsevier.com/retrieve/pii/B9780128181409000118), pp. 123–129.
  24. S. Soyk et al., Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat. Genet. 49, 162–168 (2017).
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  28. S.-N. Bai, Are unisexual flowers an appropriate model to study plant sex determination? J. Exp. Bot. (2020), doi:10.1093/jxb/eraa207.
Go to the profile of Gao Jianguo

Gao Jianguo

Dr., Peking University

Dr. Gao Jianguo (高建国, 博士) mainly focuses on (but not limited to): plant-water relations, plant physiological ecology, tree physiology & ecosystem ecology. He graduated from Chinese Academy of Sciences (CAS) in 2015 and turned to a well-trained scientist. His interests actually are very wide and wild, most of them constrained in plant and ecology. He was well-trained in science and as the first author published several peer-reviewed papers.

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Gao Jianguo 28 days ago

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