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Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 December 2019) | Viewed by 36796

Special Issue Editors


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Guest Editor
Departamento de Fisiología, Anatomía y Biología Celular, Universidad Pablo de Olavide, E-41013 Sevilla, Spain
Interests: plant boron
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Guest Editor
Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan
Interests: boron; transport; translational regulation; boron stress tolerance

Special Issue Information

Dear Colleagues,

Boron is an essential element for vascular plants. The requirement for boron in many phases of plant development is well recognized, but the mechanisms underlying this essentiality have proven difficult to establish. There is clear evidence for a role of boron in the cross-linking of the rhamnogalacturonan II complex between pectic polysaccharides in plant cell walls, but compelling evidence for the participation of boron in other cellular activities is currently challenging. The involvement of boron in signaling has also been proposed to explain some of the multitude of changes in cellular activities induced by boron deficiency and toxicity.

Plants differ greatly in their ability to utilize boron and to tolerate excess boron. Physiological and molecular studies have demonstrated that much of this variability can be explained by differences in the uptake and distribution of boron in plants, which is primarily controlled by a suite of membrane transporters. Considerable progress has been made in identifying the location of these transporters and the conditions that control their expression.

Both boron deficiency and toxicity are major management issues in agriculture and there is clearly a need for greater research to understand how boron supply can best be manipulated to optimize crop production. Central to this aim is the need to better understand the metabolic and structural functions of boron, the importance of membrane transport, and whether boron also has a major signaling role.

We invite investigators to contribute original research and review articles in the field of boron in plants. Papers focused on boron in agriculture as well as describing new technical approaches regarding boron are also welcome.

Prof. Dr. Agustín González-Fontes
Prof. Dr. Toru Fujiwara
Guest Editors

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Keywords

  • Boron in soils and aquatic environments
  • Boron uptake and translocation
  • Boron functions: cell wall, membranes, cytosol, and organelles
  • Boron deficiency: effects and mechanisms for tolerance
  • Boron toxicity: effects and mechanisms for tolerance
  • Boron toxicity and salt stress
  • Boron and gene transcription
  • Boron and cell signaling
  • Boron and agriculture

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Published Papers (7 papers)

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Editorial

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3 pages, 187 KiB  
Editorial
Advances in Plant Boron
by Agustín González-Fontes and Toru Fujiwara
Int. J. Mol. Sci. 2020, 21(11), 4107; https://doi.org/10.3390/ijms21114107 - 9 Jun 2020
Cited by 10 | Viewed by 2495
Abstract
Although very recently, David H [...] Full article
(This article belongs to the Special Issue Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction)

Research

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16 pages, 1794 KiB  
Article
Assessment of a 18F-Phenylboronic Acid Radiotracer for Imaging Boron in Maize
by Alexandra B. Housh, Michaela S. Matthes, Amber Gerheart, Stacy L. Wilder, Kun-Eek Kil, Michael Schueller, James M. Guthrie, Paula McSteen and Richard Ferrieri
Int. J. Mol. Sci. 2020, 21(3), 976; https://doi.org/10.3390/ijms21030976 - 1 Feb 2020
Cited by 11 | Viewed by 3568
Abstract
Boron (B) is an essential plant micronutrient. Deficiencies of B have drastic consequences on plant development leading to crop yield losses and reductions in root and shoot growth. Understanding the molecular and cellular consequences of B deficiency is challenging, partly because of the [...] Read more.
Boron (B) is an essential plant micronutrient. Deficiencies of B have drastic consequences on plant development leading to crop yield losses and reductions in root and shoot growth. Understanding the molecular and cellular consequences of B deficiency is challenging, partly because of the limited availability of B imaging techniques. In this report we demonstrate the efficacy of using 4-fluorophenylboronic acid (FPBA) as a B imaging agent, which is a derivative of the B deficiency mimic phenylboronic acid (PBA). We show that radioactively labelled [18F]FPBA (t½=110 m) accumulates at the root tip, the root elongation zone and at lateral root initiation sites in maize roots, and also translocates to the shoot where it accumulates along the leaf edges. Treatment of maize seedlings using FPBA and PBA causes a shortened primary root phenotype with absence of lateral roots in a dose-dependent manner. The primary root defects can be partially rescued by the addition of boric acid indicating that PBA can be used to induce B deficiency in maize and that radioactively labelled FPBA can be used to image sites of B demand on a tissue level. Full article
(This article belongs to the Special Issue Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction)
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20 pages, 5554 KiB  
Article
Genome-Wide Identification of Long Non-coding RNA in Trifoliate Orange (Poncirus trifoliata (L.) Raf) Leaves in Response to Boron Deficiency
by Gao-Feng Zhou, Li-Ping Zhang, Bi-Xian Li, Ou Sheng, Qing-Jiang Wei, Feng-Xian Yao, Guan Guan and Gui-Dong Liu
Int. J. Mol. Sci. 2019, 20(21), 5419; https://doi.org/10.3390/ijms20215419 - 31 Oct 2019
Cited by 17 | Viewed by 3142
Abstract
Long non-coding RNAs (lncRNAs) play important roles in plant growth and stress responses. As a dominant abiotic stress factor in soil, boron (B) deficiency stress has impacted the growth and development of citrus in the red soil region of southern China. In the [...] Read more.
Long non-coding RNAs (lncRNAs) play important roles in plant growth and stress responses. As a dominant abiotic stress factor in soil, boron (B) deficiency stress has impacted the growth and development of citrus in the red soil region of southern China. In the present work, we performed a genome-wide identification and characterization of lncRNAs in response to B deficiency stress in the leaves of trifoliate orange (Poncirus trifoliata), an important rootstock of citrus. A total of 2101 unique lncRNAs and 24,534 mRNAs were predicted. Quantitative real-time polymerase chain reaction (qRT-PCR) experiments were performed for a total of 16 random mRNAs and lncRNAs to validate their existence and expression patterns. Expression profiling of the leaves of trifoliate orange under B deficiency stress identified 729 up-regulated and 721 down-regulated lncRNAs, and 8419 up-regulated and 8395 down-regulated mRNAs. Further analysis showed that a total of 84 differentially expressed lncRNAs (DELs) were up-regulated and 31 were down-regulated, where the number of up-regulated DELs was 2.71-fold that of down-regulated. A similar trend was also observed in differentially expressed mRNAs (DEMs, 4.21-fold). Functional annotation of these DEMs was performed using Gene Ontology (GO) and the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses, and the results demonstrated an enrichment of the categories of the biosynthesis of secondary metabolites (including phenylpropanoid biosynthesis/lignin biosynthesis), plant hormone signal transduction and the calcium signaling pathway. LncRNA target gene enrichment identified several target genes that were involved in plant hormones, and the expression of lncRNAs and their target genes was significantly influenced. Therefore, our results suggest that lncRNAs can regulate the metabolism and signal transduction of plant hormones, which play an important role in the responses of citrus plants to B deficiency stress. Co-expression network analysis indicated that 468 significantly differentially expressed genes may be potential targets of 90 lncRNAs, and a total of 838 matched lncRNA-mRNA pairs were identified. In summary, our data provides a rich resource of candidate lncRNAs and mRNAs, as well as their related pathways, thereby improving our understanding of the role of lncRNAs in response to B deficiency stress, and in symptom formation caused by B deficiency in the leaves of trifoliate orange. Full article
(This article belongs to the Special Issue Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction)
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21 pages, 4277 KiB  
Article
Boron Deficiency Effects on Sugar, Ionome, and Phytohormone Profiles of Vascular and Non-Vascular Leaf Tissues of Common Plantain (Plantago major L.)
by Benjamin Pommerrenig, Kai Eggert and Gerd P. Bienert
Int. J. Mol. Sci. 2019, 20(16), 3882; https://doi.org/10.3390/ijms20163882 - 9 Aug 2019
Cited by 24 | Viewed by 5625
Abstract
Vascular tissues essentially regulate water, nutrient, photo-assimilate, and phytohormone logistics throughout the plant body. Boron (B) is crucial for the development of the vascular tissue in many dicotyledonous plant taxa and B deficiency particularly affects the integrity of phloem and xylem vessels, and, [...] Read more.
Vascular tissues essentially regulate water, nutrient, photo-assimilate, and phytohormone logistics throughout the plant body. Boron (B) is crucial for the development of the vascular tissue in many dicotyledonous plant taxa and B deficiency particularly affects the integrity of phloem and xylem vessels, and, therefore, functionality of long-distance transport. We hypothesize that changes in the plants’ B nutritional status evoke differential responses of the vasculature and the mesophyll. However, direct analyses of the vasculature in response to B deficiency are lacking, due to the experimental inaccessibility of this tissue. Here, we generated biochemical and physiological understanding of B deficiency response reactions in common plantain (Plantago major L.), from which pure and intact vascular bundles can be extracted. Low soil B concentrations affected quantitative distribution patterns of various phytohormones, sugars and macro-, and micronutrients in a tissue-specific manner. Vascular sucrose levels dropped, and sucrose loading into the phloem was reduced under low B supply. Phytohormones responded selectively to B deprivation. While concentrations of abscisic acid and salicylic acid decreased at low B supply, cytokinins and brassinosteroids increased in the vasculature and the mesophyll, respectively. Our results highlight the biological necessity to analyze nutrient deficiency responses in a tissue- rather organ-specific manner. Full article
(This article belongs to the Special Issue Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction)
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16 pages, 3282 KiB  
Article
Boron Deficiency Increases Cytosolic Ca2+ Levels Mainly via Ca2+ Influx from the Apoplast in Arabidopsis thaliana Roots
by Carlos Quiles-Pando, M. Teresa Navarro-Gochicoa, M. Begoña Herrera-Rodríguez, Juan J. Camacho-Cristóbal, Agustín González-Fontes and Jesús Rexach
Int. J. Mol. Sci. 2019, 20(9), 2297; https://doi.org/10.3390/ijms20092297 - 9 May 2019
Cited by 18 | Viewed by 3649
Abstract
Boron (B) is a micronutrient for plant development, and its deficiency alters many physiological processes. However, the current knowledge on how plants are able to sense the B-starvation signal is still very limited. Recently, it has been reported that B deprivation induces an [...] Read more.
Boron (B) is a micronutrient for plant development, and its deficiency alters many physiological processes. However, the current knowledge on how plants are able to sense the B-starvation signal is still very limited. Recently, it has been reported that B deprivation induces an increase in cytosolic calcium concentration ([Ca2+]cyt) in Arabidopsis thaliana roots. The aim of this work was to research in Arabidopsis whether [Ca2+]cyt is restored to initial levels when B is resupplied and elucidate whether apoplastic Ca2+ is the major source for B-deficiency-induced rise in [Ca2+]cyt. The use of chemical compounds affecting Ca2+ homeostasis showed that the rise in root [Ca2+]cyt induced by B deficiency was predominantly owed to Ca2+ influx from the apoplast through plasma membrane Ca2+ channels in an IP3-independent manner. Furthermore, B resupply restored the root [Ca2+]cyt. Interestingly, expression levels of genes encoding Ca2+ transporters (ACA10, plasma membrane PIIB-type Ca2+-ATPase; and CAX3, vacuolar cation/proton exchanger) were upregulated by ethylene glycol tetraacetic acid (EGTA) and abscisic acid (ABA). The results pointed out that ACA10, and especially CAX3, would play a major role in the restoration of Ca2+ homeostasis after 24 h of B deficiency. Full article
(This article belongs to the Special Issue Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction)
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16 pages, 1446 KiB  
Article
MicroRNA Sequencing Revealed Citrus Adaptation to Long-Term Boron Toxicity through Modulation of Root Development by miR319 and miR171
by Jing-Hao Huang, Xiong-Jie Lin, Ling-Yuan Zhang, Xian-Da Wang, Guo-Cheng Fan and Li-Song Chen
Int. J. Mol. Sci. 2019, 20(6), 1422; https://doi.org/10.3390/ijms20061422 - 21 Mar 2019
Cited by 35 | Viewed by 3633
Abstract
Boron (B) toxicity in Citrus is a common physiological disorder leading to reductions in both productivity and quality. Studies on how Citrus roots evade B toxicity may provide new insight into plant tolerance to B toxicity. Here, using Illumina sequencing, differentially expressed microRNAs [...] Read more.
Boron (B) toxicity in Citrus is a common physiological disorder leading to reductions in both productivity and quality. Studies on how Citrus roots evade B toxicity may provide new insight into plant tolerance to B toxicity. Here, using Illumina sequencing, differentially expressed microRNAs (miRNAs) were identified in B toxicity-treated Citrus sinensis (tolerant) and C. grandis (intolerant) roots. The results showed that 37 miRNAs in C. grandis and 11 miRNAs in C. sinensis were differentially expressed when exposed to B toxicity. Among them, miR319, miR171, and miR396g-5p were confirmed via 5′-RACE and qRT-PCR to target a myeloblastosis (MYB) transcription factor gene, a SCARECROW-like protein gene, and a cation transporting ATPase gene, respectively. Maintenance of SCARECROW expression in B treated Citrus roots might fulfill stem cell maintenance, quiescent center, and endodermis specification, thus allowing regular root elongation under B-toxic stress. Down-regulation of MYB due to up-regulation of miR319 in B toxicity-treated C. grandis roots might decrease the number of root tips, thereby dramatically changing root system architecture. Our findings suggested that miR319 and miR171 play a pivotal role in Citrus adaptation to long-term B toxicity by targeting MYB and SCARECROW, respectively, both of which are responsible for root growth and development. Full article
(This article belongs to the Special Issue Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction)
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Review

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20 pages, 404 KiB  
Review
Boron Toxicity and Deficiency in Agricultural Plants
by Milka Brdar-Jokanović
Int. J. Mol. Sci. 2020, 21(4), 1424; https://doi.org/10.3390/ijms21041424 - 20 Feb 2020
Cited by 257 | Viewed by 13611
Abstract
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Novel Aspects of Boron Biology in Plants. Boron and Plant Interaction)
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