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Frond Architecture of the Rootless Duckweed Wolffia Globosa Jingjing Yang1, Xuyao Zhao1, Gaojie Li1, Shiqi Hu1,2 and Hongwei Hou1*

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Frond Architecture of the Rootless Duckweed Wolffia Globosa Jingjing Yang1, Xuyao Zhao1, Gaojie Li1, Shiqi Hu1,2 and Hongwei Hou1* Yang et al. BMC Plant Biology (2021) 21:387 https://doi.org/10.1186/s12870-021-03165-5 RESEARCH ARTICLE Open Access Frond architecture of the rootless duckweed Wolffia globosa Jingjing Yang1, Xuyao Zhao1, Gaojie Li1, Shiqi Hu1,2 and Hongwei Hou1* Abstract Background: The plant body in duckweed species has undergone reduction and simplification from the ancient Spirodela species towards more derived Wolffia species. Among the five duckweed genera, Wolffia members are rootless and represent the smallest and most reduced species. A better understanding of Wolffia frond architecture is necessary to fully explore duckweed evolution. Results: We conducted a comprehensive study of the morphology and anatomy of Wolffia globosa, the only Wolffia species in China. We first used X-ray microtomography imaging to reveal the three-dimensional and internal structure of the W. globosa frond. This showed that new fronds rapidly budded from the hollow reproductive pocket of the mother fronds and that several generations at various developmental stages could coexist in a single W. globosa frond. Using light microscopy, we observed that the meristem area of the W. globosa frond was located at the base of the reproductive pocket and composed of undifferentiated cells that continued to produce new buds. A single epidermal layer surrounded the W. globosa frond, and the mesophyll cells varied from small and dense palisade-like parenchyma cells to large, vacuolated cells from the ventral to the dorsal part. Furthermore, W. globosa fronds contained all the same organelles as other angiosperms; the most prominent organelles were chloroplasts with abundant starch grains. Conclusions: Our study revealed that the reproductive strategy of W. globosa plants enables the rapid accumulation of biomass and the wide distribution of this species in various habitats. The reduced body plan and size of Wolffia are consistent with our observation that relatively few cell types are present in these plants. We also propose that W. globosa plants are not only suitable for the study of structural reduction in higher plants, but also an ideal system to explore fundamental developmental processes of higher plants that cannot be addressed using other model plants. Keywords: Wolffia globosa, Morphology, Three-dimensional structure, Light microscopy, Ultrastructure Background attentions for their economic value and potential to Duckweeds, aquatic monocotyledonous plants of the ameliorate resource limitations and environmental prob- family Lemnaceae, include five genera (Spirodela, Land- lems [3]. For example, duckweeds are widely used for oltia, Lemna, Wolffiella,andWolffia) with variable standardized toxicity testing of various water contami- morphologies and living habits, propagating mostly by nants including nitrogen, phosphorus, metals, and nu- vegetative reproduction [1, 2]. Duckweeds have attracted merous organic compounds [4, 5]. Duckweeds also possess good qualitative and quantitative nutritional pro- files without detectable anti-proliferative or cytotoxic ef- * Correspondence: [email protected] 1The State Key Laboratory of Freshwater Ecology and Biotechnology, The Key fects and could serve as a new source of human food [6]. Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Duckweed-based expression systems with strictly con- Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan trolled formats have been developed to produce various 430072, China Full list of author information is available at the end of the article recombinant proteins with relatively high yield [7, 8]. © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Yang et al. BMC Plant Biology (2021) 21:387 Page 2 of 10 Duckweeds also may be valuable feedstock for biofuel species, which lack pseudoroots [19]. These previous production due to their high biomass and starch accu- studies demonstrated that members of the Wolffia genus mulation [9, 10]. Furthermore, their rapid growth rate, vary distinctively in morphology, anatomy, growth etc. ease of cultivation and transformation, direct contact in adaption to different living environments. with water, and ability to adapt to environmental Wolffia globosa is the only Wolffia species in China changes make duckweeds suitable plant models and ex- [20] and it has a genome size of 1300 Mbp [12]. Stable cellent materials for physiological studies [3]. and transient transformation methods for W. globosa Duckweeds have undergone reduction and simplifica- have been established [21]. Based on this efficient gen- tion of the plant body from the ancient Spirodela species etic transformation system, W. globosa has been used to towards the more-derived Wolffia species [11]. Among express a protective edible vaccine antigen against fish the five duckweed genera, Wolffia members are rootless vibriosis with high survival of vaccinated fish (63.3%), and represent the smallest (0.5–1 mm) and most- which indicated that W. globosa could serve as a bioreac- reduced species; other duckweed species (including Spir- tor to produce edible vaccines [7]. W. globosa is also a odela, Landoltia,andLemna) produce adventitious good indicator of metal pollution in aquatic environ- roots. DNA content estimates also vary nearly thirteen- ments [22, 23]. Early studies by Landolt [11] reported fold among duckweed species, ranging from 158 Mbp in the morphology of W. globosa. Huang [20] studied the Spirodela polyrhiza to 1881Mbp in Wolffia arrhiza [12], phylogeny and genetic diversity of W. globosa in China and negatively correlate with body size [12–14]. The based on sequencing of the mat-K gene and random striking variation in body plan and size among duck- amplified polymorphic DNA (RAPD) markers. Huang weeds is one of the most extreme examples of structural [20] also preliminaily compared the anatomy of the tur- reduction in any family. However, we lack knowledge ion, frond, and flowering structures among W. globosa about the mechanisms driving its occurrence within the individuals from the field. The morphology and anatomy plant kingdom. of W. globosa still need further investigation to reveal its Two studies by Landolt [11] described the morphology unique characteristics that may be of importance in of the Wolffia genus and characterized its members basic and applied research. Here, we report a compre- based on their frond shape, frond width, number of sto- hensive study of the morphology and anatomy of W. glo- mata, stigma with or without pigment cells, etc. Ander- bosa. The findings provide a foundation for future son et al. [15] first reported the light and electron research on duckweed growth, development, physiology, microscopic structure of the W. arrhiza frond, revealing and evolution. Biological research on duckweeds is that W. arrhiza fronds varied considerably from mature growing as genomes of some duckweed species have chlorenchymous tissue to the meristematic area where been sequenced [24]. We hope to attract more investiga- numerous daughter fronds develop. The frond structure tors and investors to join our efforts and realize the of Wolffia australiana was similar to that of W. arrhiza; great potential of duckweed as a model system for basic however, the W. australiana chloroplasts were concen- and applied research in plants. trated in dorsal mesophyll cells [16]. White and Wise [17] revealed the differences in mesophyll anatomies be- Results tween Wolffia columbiana and Wolffia borealis: the Morphology of the W. globosa frond chloroplasts were located mainly in the epidermis of W. The three-dimensional (3D) volumes of the W. globosa columbiana with a single mesophyll cell size and type, frond are shown in Fig. 1 and Movie S1. The oval- but were concentrated in the dorsal part of W. borealis shaped W. globosa frond could be divided into dorsal, with a steep gradient in cell size, as in W. australiana ventral, and lateral parts (Fig. 1A1). There was one big and W. arrhiza. Lemon and Posluszny [18] were the first cavity in both the mother frond (MF) and daughter to compare the developmental morphology of shoots in frond (DF1) named the reproductive pocket (RpM and S. polyrhiza, Lemna minor, and W. borealis, which re- RpD, respectively) (Fig. 1A2–A5). The MF had two vis- vealed the successive formation of new generations in ible daughter fronds (DF1 and DF2), one (DF2) budding these three duckweed species and their progressive sim- from the base of the RpM. The DF1 also had two new plification from Spirodela to Lemna to Wolffia. Sree buds (GF1 and GF2) (Fig. 1A3–A5). The empty RpM et al. [19] reported the unique morphology of vegetative with the new bud (DF2) was exposed when the attached and generative propagation in Wolffia microscopica daughter frond (DF1) was separated (Fig. 1B2–B5). It using light and electron microscopy. They observed was located at one end of the MF and opened when DF1 flowering in different generations of W. microscopica at protruded from the MF. Stomata were found only in the the same time [19]. Furthermore, W. microscopica dorsal part of the frond; no stoma were found in the fronds often possessed a ventral projection and a special ventral and lateral parts (Fig.
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