Boron deficiency disorders the cell wall in Neolamarckia cadamba
Introduction
Neolamarckia cadamba (Roxb.) Bosser is a multifunctional, fast-growing tree species that is widely used as a type of medicine in some Asian countries (Ouyang et al., 2016). Recent transcriptome-based studies and structural analysis have provided insight into the characterization of heteroxylan biosynthesis and woody tissue formation in N. cadamba (Zhao et al., 2014, Zhao et al., 2017).
Boron (B) was classified as an essential element in 1923 (Warington, 1923), and the demand for B varies between different plants and even different tissues. B demand in plants is trace, but B deficiency usually induces incurable symptoms. Representative symptoms induced by B deficiency include stunted growth, swelling growing tips, death of growing tips in severe cases, and curled leaves with yellow spotting (Matoh, 1997, Brown et al., 2008). All these changes severely impact both the quality and production of commercially important plants (Brown et al., 2002). Overall cell wall changes under B deficiency in timber plant are still rarely reported.
Nearly 90% of cellular B is positioned on the cell wall (Loomis and Durst, 1992), and nearly four-fifths of the cell wall B is just bound to polysaccharides containing cis diol substrates (Matoh, 1997). It is well known that B influences the mechanical properties of intercellular pectins. Two chains of monomeric RGII, Ca2+, and two molecules of B make a covalent complex B-RGII as a part of pectins structure that affects cell-to-cell adhesion (Loomis and Durst, 1992, Matoh, 1997, O'Neill et al., 2004). UDP-D-apiose/UDP-D-xylose synthase (AXS) which is participated in regulating apiose content plays an important role in RGII cross-linking with B. The Arabidopsis axs1 axs2/+ mutant contains less B-RGII dimers (Zhao et al., 2020), and AXS1-silenced plants by virus induced gene silencing (VIGS) are dwarfed (Ahn et al., 2006), indicating that B-RGII is vital for normal morphogenesis. Pectin hydrolases, polygalacturonases, pectin lyase, and pectin methyl esterase biodegrade glycosidic bonds of pectic substances and disintegrate the cell wall (Fogarty and Kelly, 1983), which led to altered expression in the Arabidopsis axs1 axs2/+ mutant (Zhao et al., 2020). Recent studies reveal the RHAMNOGALACTURONAN XYLOSYLTRANSFERASE (RGXT) family including RGXT1, RGXT2 and RGXT3 possess α-1, 3-xylosyltransferase activity and can transfer Xyl from UDP-Xyl onto Fuc, and this linkage is peculiar to RGII (Petersen et al., 2009, Harholt et al., 2010). The influence of B-RGII to RGXT is still unclear. B-bridging implicates other pectic composition changes, which was needed.
B may also be required for lignin biosynthesis according to the land plants origin and numerous studies (Kutschera and Niklas, 2017, Lewis, 1980). Lignin, the second most abundant polymer in plant cell walls, is synthesized by the conversion of phenylalanine to cinnamate and a series of methylations, hydroxylations and oxidation. Plants under B deficiency have lignification and thick cell walls (Dutta and McIlrath, 1964, Slack and Whittington, 1964). The plant cell wall is an unbroken structure, and its integrity can affect disease resistance. Cellulose is the most characteristic, and is involved in differential defence responses (Bacete et al., 2018). For example, Arabidopsis cellulose synthase CESA4, CESA7, and CESA8 have been shown to enhance resistance to different pathogens (Desprez et al., 2007, Escudero et al., 2017, Hernández-Blanco et al., 2007).
As a movable element, B transporters fall into two groups. One group consists of BORs exporting B from cell to cell, and the other group consists of NIPs which enhance bidirectional permeability (Sotta et al., 2017). Transport protein levels seem to depend on B concentration. While it is now clear that the borate receptor BOR1/2 may have partially similar pathways to perform its function, it is not yet clear whether there are any analogous mechanisms in woody plants.
In this study, we investigate nutrient content and antioxidant enzyme activities in leaves of Neolamarckia cadamba growing under B deficiency. Next, we study the lignification of the first internode. Water-soluble pectin content and gene expression patterns of pectin biosynthesis and degradation show B deficiency cause pectin content to decrease. We also find that cellulose biosynthesis also changes with B deficiency. Our research confirms that B deficiency not only affects pectin (B-RGII), but also the other cell wall components lignin and cellulose in N. cadamba.
Section snippets
Plant materials and culture
To ensure consistency and clarity between experiments, plantlets of Neolamarckia cadamba were cultured by tissue culture. Three-month-old plantlets were grown in Hoagland’s nutrient cultured solution in distilled water supplemented with the following concentrations of macro- and micro-nutrients; 1.6 mmol L-1 (mM) Ca (NO3)2, 2.4 mM KNO3, 0.8 mM MgSO4, 0.4 mM NH4H2PO4, 38 μmol L-1 (μΜ) MnSO4, 0.32 μM ZnSO4, 0.12 μM CuSO4, 0.008 μM (NH4)6Mo7O24 and 32 μM FeNa-EDTA, as B0. The experimental setup
B deficiency exhibited effects on plant growth and morphology
In order to examine B function in N. cadamba growth, three-month-old seedlings were treated on Hydroponics Hoagland’s nutrient cultured solution system without B (B0) and with 20 μM B (B20). Compared to B20, B0 severely hampered the growth of vegetative morphology (stems, shoot tips and leaves) in N. cadamba. Plantlets grown on B deficiency culture solution were shorter than those in B20 (Fig. 1A). These had partially thick and black stems with withered shoot tips due to cell death (Fig. 1B),
Discussion
Although B is a micro-element of plants, it plays an indispensable role in regulating plant metabolism and growth (Papadakis et al., 2018, Riaz et al., 2018). It is very difficult to explore the impact of B deficiency effects on plant development, especially for wood. Growing trees in a hydroponic system makes it possible to study the mechanism of B effects on wood plants by comparing physiology analysis, cell wall composition, ionic concentration, osmotic pressure, nutritive elements and gene
Conclusions
Based on morpho-physiological observations and assays, biophysical examinations and transcriptional analyses, our results illustrate that cell wall lignification, changes of pectin and up-regulation of cellulose genes occurs in response to B deficiency in N. cadamba. Decreased pectin concentration as well as up-regulation of genes encoding PG and BGAL indicate that B deficiency directly impacts pectin in N. cadamba. Furthermore, up-regulation of cellulose synthase genes provides a new basis to
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
Financial support for this work was obtained by Key Project of Guangzhou Science and Technology Plan (201904020014), China and the National Natural Science Foundation of China (Grant Numbers 31870653, 31670670, 31811530009, 31670601).
Authors’ contributions
A. W. and X. D. design the experiments; Q.Y. and W. Q. analyzed the data and wrote the manuscript; L. K., Y. L. and T. L. performed the experimrnts; H.L.and F. M. revised the language of the manuscript.
CRediT authorship contribution statement
Qi Yin: Data curation, Methodology, Writing − original draft. Lu Kang: Data curation, Methodology. Yi Liu: Data curation, Methodology. Mirza Faisal Qaseem: Data curation, Methodology. Wenqi Qin: Data curation, Writing − original draft. Tingting Liu: Data curation, Methodology. Huiling Li: Data curation, Methodology, Writing, Conceptualization, Supervision. Xiaomei Deng, Ai-Min Wu: Conceptualization, Supervision, Project administration, Writing − review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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