Higher Boron Accumulation is Associated with Low-Boron Tolerance in Mustard

Jothi M., Takano J.

Boron (B) is a micronutrient required for optimal plant growth and development. It is primarily involved in pectin crosslinking in the rhamnogalacturonan II region to ensure cell wall integrity. In plants grown under limited soil B availability, seed yield and quality are often compromised. However, excessive B accumulation can also be toxic to plants. Therefore, plants must maintain optimal tissue concentrations of B by regulating transport processes. This article is a critical review of the molecular mechanisms involved in B transport under limited and excess B conditions. We focus on various B transport proteins and their B-dependent regulation, mainly as studied in the model plant Arabidopsis thaliana, and summarize research progress on B transport and its regulation in Brassica napus, Oryza sativa, Hordeum vulgare, Triticum aestivum, and Zea mays. Under limited B conditions, the nodulin 26-like intrinsic protein (NIP) AtNIP5;1 and the borate transporter (BOR) AtBOR1 mediate the radial transport of boric acid or borate from soil to the xylem. AtBOR2 also plays a role in root cell elongation by increasing the B-RGII dimerization rate. Under excess B conditions, AtBOR4 is involved in the directional export of B from roots to soil. In crop plants, NIPs and BORs responsible for B efficiency and excess B tolerance are becoming key targets of plant breeding. These B transport proteins are regulated at the transcription, mRNA degradation, translational repression, and endocytic degradation levels to maintain B homeostasis. Understanding the complex regulatory mechanisms of B transport will allow us to develop high-yielding plants under fluctuating soil B conditions.

Dong X., Jiang C., Wei S., Jiao H., Ran K., Dong R., Wang S.

Boron (B) is a required micronutrient that is crucial for the growth and development of vascular plants. A deficiency in B is generally regarded as a limiting factor affecting agricultural production in many parts of the world. Boron is involved in the metabolism of plant lignin and additionally, B deficiency can lead to the excessive accumulation of lignin in plant leaves/roots, resulting in corking symptoms and inhibited growth. However, the effect of B on lignin biosynthesis is not as well characterized as the specific function of B in the cell wall. In this article, recent studies on the regulation of lignin biosynthesis in plants under low-B stress conditions are reviewed. Moreover, the following possible mechanisms underlying the lignin synthesis promoted by B deficiency are discussed: (1) the accumulation of phenolic substances during B deficiency directly enhances lignin synthesis; (2) Excess H2 O2 has a dual function to the enhancement of lignin under boron deficiency conditions, serving as a substrate and a signaling molecule; and (3) B deficiency regulates lignin synthesis through the expression of genes encoding transcription factors such as MYBs. Finally, future studies regarding physiology, molecules, and transcriptional regulation may reveal the mechanism(s) mediating the relationship between lignin synthesis and B deficiency. This review provides new insights and important references for future research and the enhancement of plant B nutrition. This article is protected by copyright. All rights reserved.

Dhaliwal S.S., Sharma V., Shukla A.K., Kaur M., Verma V., Sandhu P.S., Alsuhaibani A.M., Gaber A., Hossain A.

Indian mustard (Brassica juncea L.) is an essential oilseed crop that offers important nutrients to human beings. However, the concurrent micronutrient deficiencies including boron (B), sulfur (S), and nitrogen (N) could pose a significant threat to public health. Therefore, this study was conducted at the Punjab Agricultural University, Ludhiana, with nine treatments, i.e., T1-Control (recommended NPK only), T2- borax (0.5%) at flowering, T3-borax (1.0%) at flowering,T4- borax (0.5%) + urea (1.0%) at flowering,T5-borax (1.0%) + urea (1.0%) at flowering, T6-borax (0.5%) at flowering + capsule formation, T7-borax (1.0%) at flowering + capsule formation, T8-borax (0.5%) + urea (1.0%) at flowering + capsule formation, T9-borax (1.0%) + urea (1.0%) at flowering + Capsule formation, replicated three times in a randomized block design for 2 years (2020–2021 and 2021–2022). The foliar application of borax (1.0%) + urea (1.0%) at the flowering and capsule formation stage (treatment T9) was highly efficient in increasing food quality parameters such as crude fiber, total soluble solids (TSS), and protein content with maximum values of 3.77, 24.9, and 27.53%, respectively. Also, maximum yields of seed as well as stover for treatment T9 were 1.376 and 6.625 kg ha−1, respectively. Similarly, the results for B, S, and N concentrations in seed (27.71 mg kg−1, 17.69 mg kg−1, and 2.35%), as well as stover (25.92 mg kg−1, 17.31 mg kg−1, and 0.33%), were maximum in treatment T9. Also, B, S, and N uptake by seed (38.18 g ha−1, 24.40 g ha−1, and 32.05 Kg ha−1) and stover (172.55 g ha−1, 115.44 g ha−1, and 21.99 Kg ha−1) were maximum for the treatment T9 involving borax (1.0%) + urea (1.0%) at the flowering and capsule formation stage. Whereas, the concentration and uptake decreased in the treatments involving the sole application of borax and urea. Therefore, the application of borax (1.0%) and urea (1.0%) at the flowering and capsule formation stage significantly improved the quality parameters, seed and stover yield, nutrient concentration, and uptake over control and could be used to alleviate the B, S, and N deficiency in Indian mustard.

Shukla A.K., Behera S.K., Prakash C., Tripathi A., Patra A.K., Dwivedi B.S., Trivedi V., Rao C.S., Chaudhari S.K., Das S., Singh A.K.

Nutrient deficiencies in soil–crop contexts and inappropriate managements are the important reasons for low crop productivity, reduced nutritional quality of agricultural produce and animal/human malnutrition, across the world. The present investigation was carried out to evaluate nutrient deficiencies of sulphur (S) and micronutrients [zinc (Zn), boron (B), iron (Fe), copper (Cu) and manganese (Mn)] in agricultural soils of India for devising effective management strategies to achieve sustainable crop production, improved nutritional quality in crops and better animal/human health. A total of 2,42,827 surface (0–15 cm depth) soil samples were collected from agriculture fields of 615 districts lying in 28 states of India and were analysed for available S and micronutrients concentration. The study was carried out under the aegis of All India Coordinated Research Project on Micro- and Secondary-Nutrients and Pollutant Elements in Soils and Plants. The mean concentrations were 27.0 ± 29.9 mg kg−1 for available S, 1.40 ± 1.60 mg kg−1 for available Zn and 1.40 ± 4.70 mg kg−1 for available B, 31.0 ± 52.2 mg kg−1 for available Fe, 2.30 ± 3.50 mg kg−1 for available Cu and 17.5 ± 21.4 mg kg−1 for available Mn. There were variable and widespread deficiencies of S and micronutrients in different states. The deficiencies (acute deficient + deficient + latent deficiency) of S (58.6% of soils), Zn (51.2% of soils) and B (44.7% of soils) were higher compared to the deficiencies of Fe (19.2% of soils), Cu (11.4% of soils) and Mn (17.4% of soils). Out of 615 districts, > 50% of soils in 101, 131 and 86 districts were deficient in available S, available Zn and available B, respectively. Whereas, > 25% of soils in 83, 5 and 41 districts had deficiencies of available Fe, available Cu and available Mn, respectively. There were occurrences of 2-nutrients deficiencies such S + Zn (9.30% of soils), Zn + B (8.70% of soils), S + B (7.00% of soils) and Zn + Fe (5.80% of soils) to a greater extent compared to the deficiencies of Zn + Mn (3.40% of soils), S + Fe (3.30% of soils), Zn + Cu (2.80% of soils) and Fe + B (2.70% of soils). Relatively lower % of soils were deficient in 3-nutrients (namely S + Zn + B, S + Zn + B and Zn + Fe + B), 4-nutrients (namely Zn + Fe + Cu + Mn) and 5-nutrients (namely Zn + Fe + Cu + Mn + B) simultaneously. The information regarding the distribution of deficiencies of S and micronutrients (both single and multi-nutrients) could be used by various stakeholders for production, supply and application of right kind of fertilizers in different districts, states and agro-ecological regions of India for better crop production, crop nutritional quality, nutrient use efficiency, soil health and for tackling human and animal malnutrition.

He M., Wang S., Zhang C., Liu L., Zhang J., Qiu S., Wang H., Yang G., Xue S., Shi L., Xu F.

Boron (B) is essential for vascular plants. Rapeseed (Brassica napus) is the second leading crop source for vegetable oil worldwide, but its production is critically dependent on B supplies. BnaA3.NIP5;1 was identified as a B-efficient candidate gene in B. napus in our previous QTL fine mapping. However, the molecular mechanism through which this gene improves low-B tolerance remains elusive. Here, we report genetic variation in BnaA3.NIP5;1 gene, which encodes a boric acid channel, is a key determinant of low-B tolerance in B. napus. Transgenic lines with increased BnaA3.NIP5;1 expression exhibited improved low-B tolerance in both the seedling and maturity stages. BnaA3.NIP5;1 is preferentially polar-localized in the distal plasma membrane of lateral root cap (LRC) cells and transports B into the root tips to promote root growth under B-deficiency conditions. Further analysis revealed that a CTTTC tandem repeat in the 5’UTR of BnaA3.NIP5;1 altered the expression level of the gene, which is tightly associated with plant growth and seed yield. Field tests with natural populations and near-isogenic lines (NILs) confirmed that the varieties carried BnaA3.NIP5;1Q allele significantly improved seed yield. Taken together, our results provide novel insights into the low-B tolerance of B. napus, and the elite allele of BnaA3.NIP5;1 could serve as a direct target for breeding low-B-tolerant cultivars.

Wu X., Riaz M., Yan L., Zhang Z., Jiang C.

Boron (B) deficiency is frequently observed in citrus orchards as a major cause for loss of productivity and quality. The structural and morphological responses of roots to B deficiency have been reported in some plants. The study was conducted to get novel information about the B-deficient-induced cellular injuries and target secondary metabolites in the shikimate pathway. Fluorescent vital staining, paraffin section, transmission electron microscopy (TEM) and target metabolomics were to investigate the responses of the cell viability and structure, and target aromatic metabolites in the shikimate pathway in B-deficient trifoliate orange roots. Boron deprivation-induced ROS accumulation accelerated the membrane peroxidation, resulting in weakened cell vitality and cell rupture in roots. In addition, B deficiency increased phenylalanine (Phe), tyrosine (Try) in roots, thereby promoting the biosynthesis of salicylic acid, caffeic acid and ferulic acid. B-starvation up-regulated salicylic acid and lignin while reduced 3-indoleacetic acid (IAA) content. These adverse effects might be involved in the structural and morphological changes in B-deficient roots. What is more, the results provide a new insight into the mechanism of B deficiency-induced structural damage and elongation inhibition on roots.

Brdar-Jokanović M.

Boron is an essential plant micronutrient taken up via the roots mostly in the form of boric acid. Its important role in plant metabolism involves the stabilization of molecules with cis-diol groups. The element is involved in the cell wall and membrane structure and functioning; therefore, it participates in numerous ion, metabolite, and hormone transport reactions. Boron has an extremely narrow range between deficiency and toxicity, and inadequate boron supply exhibits a detrimental effect on the yield of agricultural plants. The deficiency problem can be solved by fertilization, whereas soil boron toxicity can be ameliorated using various procedures; however, these approaches are costly and time-consuming, and they often show temporary effects. Plant species, as well as the genotypes within the species, dramatically differ in terms of boron requirements; thus, the available soil boron which is deficient for one crop may exhibit toxic effects on another. The widely documented intraspecies genetic variability regarding boron utilization efficiency and toxicity tolerance, together with the knowledge of the physiology and genetics of boron, should result in the development of efficient and tolerant varieties that may represent a long-term sustainable solution for the problem of inadequate or excess boron supply.

Gigli-Bisceglia N., Engelsdorf T., Hamann T.

The walls surrounding the cells of all land-based plants provide mechanical support essential for growth and development as well as protection from adverse environmental conditions like biotic and abiotic stress. Composition and structure of plant cell walls can differ markedly between cell types, developmental stages and species. This implies that wall composition and structure are actively modified during biological processes and in response to specific functional requirements. Despite extensive research in the area, our understanding of the regulatory processes controlling active and adaptive modifications of cell wall composition and structure is still limited. One of these regulatory processes is the cell wall integrity maintenance mechanism, which monitors and maintains the functional integrity of the plant cell wall during development and interaction with environment. It is an important element in plant pathogen interaction and cell wall plasticity, which seems at least partially responsible for the limited success that targeted manipulation of cell wall metabolism has achieved so far. Here, we provide an overview of the cell wall polysaccharides forming the bulk of plant cell walls in both monocotyledonous and dicotyledonous plants and the effects their impairment can have. We summarize our current knowledge regarding the cell wall integrity maintenance mechanism and discuss that it could be responsible for several of the mutant phenotypes observed.

Ogden M., Hoefgen R., Roessner U., Persson S., Khan G.

Nutrients are critical for plants to grow and develop, and nutrient depletion severely affects crop yield. In order to optimize nutrient acquisition, plants adapt their growth and root architecture. Changes in growth are determined by modifications in the cell walls surrounding every plant cell. The plant cell wall, which is largely composed of complex polysaccharides, is essential for plants to attain their shape and to protect cells against the environment. Within the cell wall, cellulose strands form microfibrils that act as a framework for other wall components, including hemicelluloses, pectins, proteins, and, in some cases, callose, lignin, and suberin. Cell wall composition varies, depending on cell and tissue type. It is governed by synthesis, deposition and remodeling of wall components, and determines the physical and structural properties of the cell wall. How nutrient status affects cell wall synthesis and organization, and thus plant growth and morphology, remains poorly understood. In this review, we aim to summarize and synthesize research on the adaptation of root cell walls in response to nutrient availability and the potential role of cell walls in nutrient sensing.

Wu X., Riaz M., Yan L., Du C., Liu Y., Jiang C.

Boron (B) is a micronutrient indispensable for citrus and B deficiency causes a considerable loss of productivity and quality in China. However, studies on pectin composition and architecture of cell wall components in trifoliate orange roots under B deficiency condition are not sufficient. In this study, we investigated the alteration in pectin characteristics and the architecture of cell wall components in trifoliate orange [Poncirus trifoliata (L.) Raf.] roots under B starvation. The results showed that B-deficient roots resulted in a significant enlargement of root tips and an obvious decrease in cell wall B and uronic acid (UA) content in Na2CO3-soluble pectin compared with B-adequate roots. Meanwhile, they showed a decrease of 2-keto-3-deoxyoctanoic acid (KDO) in CDTA-soluble and Na2CO3-soluble pectin in cell walls, while the degree of methylation (DM) of CDTA-soluble pectin was significantly increased under B deficiency. Transmission electron microscope (TEM) micrographs of B deficient plants showed a distinct thickening of the cell walls, with the thickness 1.82 times greater than that of control plant roots. The results from fourier-transform infrared spectroscopy (FTIR) showed that B deficiency changed the mode of hydrogen bonding between protein and carbohydrates (cellulose and hemicellulose). The FTIR spectra exhibited a destroyed protein structure and accumulation of wax and cellulose in the cell walls under B starvation. The 13C nuclear magnetic resonance (13C-NMR) spectra showed that B starvation changed the organic carbon structure of cell walls, and enhanced the contents of amino acid, cellulose, phenols and lignin in the cell wall. The results reveal that the swelling and weakened structural integrity of cell walls, which induced by alteration on the network of pectin and cell wall components and structure in B-deficient roots, could be a major cause of occurrence of the rapid interruption of growth and significantly enlarged root tips in trifoliate orange roots under B-insufficient condition.

Wiercigroch E., Szafraniec E., Czamara K., Pacia M.Z., Majzner K., Kochan K., Kaczor A., Baranska M., Malek K.

Carbohydrates are widespread and naturally occurring compounds, and essential constituents for living organisms. They are quite often reported when biological systems are studied and their role is discussed. However surprisingly, up till now there is no database collecting vibrational spectra of carbohydrates and their assignment, as has been done already for other biomolecules. So, this paper serves as a comprehensive review, where for selected 14 carbohydrates in the solid state both FT-Raman and ATR FT-IR spectra were collected and assigned. Carbohydrates can be divided into four chemical groups and in the same way is organized this review. First, the smallest molecules are discussed, i.e. monosaccharides (d-(-)-ribose, 2-deoxy-d-ribose, l-(-)-arabinose, d-(+)-xylose, d-(+)-glucose, d-(+)-galactose and d-(-)-fructose) and disaccharides (d-(+)-sucrose, d-(+)-maltose and d-(+)-lactose), and then more complex ones, i.e. trisaccharides (d-(+)-raffinose) and polysaccharides (amylopectin, amylose, glycogen). Both Raman and IR spectra were collected in the whole spectral range and discussed looking at the specific regions, i.e. region V (3600-3050cm-1), IV (3050-2800cm-1) and II (1200-800cm-1) assigned to the stretching vibrations of the OH, CH/CH2 and C-O/C-C groups, respectively, and region III (1500-1200cm-1) and I (800-100cm-1) dominated by deformational modes of the CH/CH2 and CCO groups, respectively. In spite of the fact that vibrational spectra of saccharides are significantly less specific than spectra of other biomolecules (e.g. lipids or proteins), marker bands of the studied molecules can be identified and correlated with their structure.

Li M., Zhao Z., Zhang Z., Zhang W., Zhou J., Xu F., Liu X.

The main symptom of boron (B) deficiency in cotton is the formation of brown rings on leaf petioles. The objective of the present study was to determine the changes in the anatomical structure and chemical composition of petioles and photosynthesis of leaves in cotton under B deficiency. Compared to the control, B deficiency treatment resulted in large increases in the number of petioles with brown rings per plant (160.0%) and the number of rings on the petiole per functional leaf (711.1%) in cotton seedlings. The relative absorbance intensity in the fingerprint region of polysaccharide structure was decreased in petiole rings under B deficiency, while lignin contents were increased. Cotton plants mitigated the impairment of transport function in cotton petioles by increasing the areas of vascular bundles, phloem, xylem, and phloem fiber. Moreover, the stomatal conductance, photosynthetic rate, and transpiration rate in leaves were significantly decreased under B deficiency, thus impeding photosynthesis in cotton plants. Therefore, B deficiency reduces transport function in petioles and photosynthesis in leaves, and leads to the formation of noticeable brown rings on petioles of cotton seedlings.

Yadav S.N., Singh S.K., Kumar O.

Funakawa H., Miwa K.

In the present review, we describe current knowledge about synthesis of borate crosslinked rhamnogalacturonan II (RG-II) and it physiological roles. RG-II is a portion of pectic polysaccharide with high complexity, present in primary cell wall. It is composed of homogalacturonan backbone and four distinct side chains (A-D). Borate forms ester bonds with the apiosyl residues of side chain A of two RG-II monomers to generate borate dimerized RG-II, contributing for the formation of networks of pectic polysaccharides. In plant cell walls, more than 90% of RG-II are dimerized by borate under B sufficient conditions. Borate crosslinking of RG-II in primary cell walls, to our knowledge, is the only experimentally proven molecular function of boron (B), an essential trace-element. Although abundance of RG-II and B is quite small in cell wall polysaccharides, increasing evidence supports that RG-II and its borate crosslinking are critical for plant growth and development. Significant advancement was made recently on the location and the mechanisms of RG-II synthesis and borate cross-linking. Molecular genetic studies have successfully identified key enzymes for RG-II synthesis and regulators including B transporters required for efficient formation of RG-II crosslinking and consequent normal plant growth. The present article focuses recent advances on (i) RG-II polysaccharide synthesis, (ii) occurrence of borate crosslinking and (iii) B transport for borate supply to RG-II. Molecular mechanisms underlying formation of borate RG-II crosslinking and the physiological impacts are discussed.

Liu G., Dong X., Liu L., Wu L., Peng S., Jiang C.

Boron (B) is an essential microelement for vascular plants. Although it has frequently been reported that B deficiency leads to abnormal cell wall structure based on microscopic observation, what exactly occurs in the architecture of cell wall under this condition remains unknown. Navel orange plants that had been treated with different amounts of B were studied through chemical and instrumental (X-ray photoelectron spectroscopy (XPS) and Fourier-transform infrared spectroscopy (FTIR)) analyses. Curling of the leaves and leaf chlorosis were observed only in the upper leaves of B-deficient plants. Boron deficiency significantly increased the relative hemicellulose and cellulose concentrations, and decreased covalently bound pectin in both upper and lower leaves. The results from XPS spectra suggested that the chemical states of carbon and oxygen were changed by B deficiency, and these changes were more serious in the upper leaves. The band at 3417 cm −1 in the upper leaf walls shifted to 3398 cm −1 due to B deficiency, suggesting that the mode of hydrogen bonding was changed by B deficiency (only in the upper leaves). The intensity and shape of the vibrations at 1200–900 cm −1 (the fingerprint region of polysaccharides) varied substantially between B-deficient plant cell walls and the control walls, indicating that B deficiency induced changes in both the amount and assembly of component polymers of cell wall. These results imply that the amount of wall components is not decisive for B deficiency symptoms in orange plants, but that rather structural changes within these fractions are important.