Molecular, Metabolic and Physiological Responses to Boron Stress in Higher Plants

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Response to Abiotic Stress and Climate Change".

Deadline for manuscript submissions: closed (20 January 2023) | Viewed by 21294

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Guest Editor
Department of Physiology, Anatomy, and Cellular Biology; Pablo de Olavide University, 41013 Seville, Spain
Interests: abiotic stress; boron in plants; boron stress tolerance; gene regulation; plant nutrition

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Guest Editor
Department of Biology, Universidad Autónoma de Madrid, Madrid, Spain
Interests: nature; gastronomy; plant science; reading
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Special Issue Information

Dear Colleagues,

Even though the first evidence of the essentiality of boron (B) for the normal development and growth of higher plants was described almost a century ago, the mechanisms underlying this essentiality has not yet been exhaustively clarified. To date, the only evidence for a direct involvement of B in plant metabolism comes from its structural role in the cell wall through the formation of ester bonds between the borate anion and apiose residues of two molecules of rhamnogalacturonan II.

B is a micronutrient that frequently shows a very narrow range of optimal concentrations; therefore, plants have evolved mechanisms to cope with deficiency and excess of B. Consistent evidence demonstrates that the maintenance of B homeostasis, which is mainly based on the active regulation of intracellular localization and the abundance of B transporters, is one of the most important mechanisms of B stress tolerance. This is supported by the following facts: (i) much of the genotypic variation regarding the ability to tolerate both B deficiency and toxicity can be explained by differences in the activity of boron transporters or their regulation, and (ii) manipulation of B transporters has made it possible to obtain transgenic plants tolerant to limited or toxic B levels.

The knowledge of the molecular, metabolic, and physiological changes induced by B deficiency or toxicity, as well as the characterization of the signaling pathways for these responses, has also advanced greatly in recent years. For instance, recent studies revealed the involvement of hormones (including ethylene, auxin, cytokinin, brassinosteroids and ABA), calcium, and reactive oxygen species in the orchestrated signaling pathways of B stress responses. Findings in these fields can contribute not only to a better understanding of the role of B in plants, but also to provide efficient strategies to improve B stress tolerance in plants.

The aim of this Special Issue is to collect findings related to these topics. Original research papers and reviews are welcome.

Dr. Juan J. Camacho-Cristóbal
Dr. Maria Reguera
Guest Editors

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Keywords

  • boron homeostasis
  • boron deficiency
  • boron toxicity
  • boron transport
  • boron functions
  • tolerance to B deficiency and toxicity

Published Papers (9 papers)

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Editorial

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4 pages, 244 KiB  
Editorial
Molecular, Metabolic and Physiological Responses to Boron Stress in Higher Plants
by María Reguera and Juan José Camacho-Cristóbal
Plants 2023, 12(11), 2136; https://doi.org/10.3390/plants12112136 - 28 May 2023
Cited by 1 | Viewed by 1005
Abstract
Although the essentiality of boron (B) for plant growth has recently been questioned [...] Full article

Research

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11 pages, 928 KiB  
Article
Silicon Differently Affects Apoplastic Binding of Excess Boron in Wheat and Sunflower Leaves
by Jasna Savic, Jelena Pavlovic, Milos Stanojevic, Predrag Bosnic, Ljiljana Kostic Kravljanac, Nina Nikolic and Miroslav Nikolic
Plants 2023, 12(8), 1660; https://doi.org/10.3390/plants12081660 - 15 Apr 2023
Cited by 3 | Viewed by 1141
Abstract
Monocots and dicots differ in their boron (B) requirement, but also in their capacity to accumulate silicon (Si). Although an ameliorative effect of Si on B toxicity has been reported in various crops, differences among monocots and dicots are not clear, in particular [...] Read more.
Monocots and dicots differ in their boron (B) requirement, but also in their capacity to accumulate silicon (Si). Although an ameliorative effect of Si on B toxicity has been reported in various crops, differences among monocots and dicots are not clear, in particular in light of their ability to retain B in the leaf apoplast. In hydroponic experiments under controlled conditions, we studied the role of Si in the compartmentation of B within the leaves of wheat (Triticum vulgare L.) as a model of a high-Si monocot and sunflower (Helianthus annuus L.) as a model of a low-Si dicot, with the focus on the leaf apoplast. The stable isotopes 10B and 11B were used to investigate the dynamics of cell wall B binding capacity. In both crops, the application of Si did not affect B concentration in the root, but significantly decreased the B concentration in the leaves. However, the application of Si differently influenced the binding capacity of the leaf apoplast for excess B in wheat and sunflower. In wheat, whose capacity to retain B in the leaf cell walls is lower than in sunflower, the continuous supply of Si is crucial for an enhancement of high B tolerance in the shoot. On the other hand, the supply of Si did not contribute significantly in the extension of the B binding sites in sunflower leaves. Full article
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13 pages, 1260 KiB  
Article
Response of Maize (Zea mays L.) to Drought under Salinity and Boron Stress in the Atacama Desert
by Camilo Riveros-Burgos, Richard Bustos-Peña, Wladimir Esteban-Condori and Elizabeth Bastías
Plants 2023, 12(7), 1519; https://doi.org/10.3390/plants12071519 - 31 Mar 2023
Cited by 3 | Viewed by 1412
Abstract
The Lluta valley in northern Chile is a hyper-arid region with annual precipitation lower than 1.1 mm, and high levels of boron (B) from alluvial deposits are present together with other salts that originated from the Cretaceous. Under these abiotic conditions, the ‘lluteño’ [...] Read more.
The Lluta valley in northern Chile is a hyper-arid region with annual precipitation lower than 1.1 mm, and high levels of boron (B) from alluvial deposits are present together with other salts that originated from the Cretaceous. Under these abiotic conditions, the ‘lluteño’ maize (Zea mays L.) is of interest because it has adapted to the Lluta valley with high salinity levels and B excess in the soil and irrigation water. Water and salt stress coincide in heavily irrigated hyper-arid agricultural areas, yet they are usually studied in isolation. We investigated in field conditions the combined effects of drought (22 days with no irrigation) under salinity (ECe: 5.5 mS cm−1; Na+: 17.8 meq L−1) and B (21.1 meq L−1) stress on physiology, growth, yield, and hourly water relations. The results allow to hypothesize that the measurement of the pre-dawn water potential represents the balance between the water potential of the soil and the root. Besides, under drought a significant effect of irrigation and time interaction was observed presenting a high differential between the leaf and stem water potential in both phenological stages. Furthermore, a decrease in net assimilation was observed, and it could be explained in part by non-stomatal factors such as the high radiation and temperature observed at the end of the season. Despite the drought, the cobs did not present a significantly lower quality compared to the cobs of plants without stress. Full article
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18 pages, 3543 KiB  
Article
Crosstalk of Cytokinin with Ethylene and Auxin for Cell Elongation Inhibition and Boron Transport in Arabidopsis Primary Root under Boron Deficiency
by María Begoña Herrera-Rodríguez, Juan José Camacho-Cristóbal, Rafael Barrero-Rodríguez, Jesús Rexach, María Teresa Navarro-Gochicoa and Agustín González-Fontes
Plants 2022, 11(18), 2344; https://doi.org/10.3390/plants11182344 - 08 Sep 2022
Cited by 6 | Viewed by 2263
Abstract
Several studies have shown the role of phytohormones in the regulation of root growth of Arabidopsis plants under boron (B) deficiency. Ethylene and auxin play an important role in the control of Arabidopsis primary root cell elongation under short-term B deprivation, whereas cytokinins [...] Read more.
Several studies have shown the role of phytohormones in the regulation of root growth of Arabidopsis plants under boron (B) deficiency. Ethylene and auxin play an important role in the control of Arabidopsis primary root cell elongation under short-term B deprivation, whereas cytokinins regulate root growth inhibition under B deficiency by controlling meristem cell proliferation. In this work, we study the possible interaction among cytokinin, ethylene, and auxin in the primary root response to B-deprivation treatment, as well as their possible role in B uptake and transport. Wild type (WT) and two mutants related to auxin and ethylene (aux1 and acs11) Arabidopsis plants were grown in control (10 µM B) or B starvation (0 µM B) treatment, in the absence or presence of trans-zeatin, and their primary root growth was analyzed. The possible interaction between these hormones was also studied by analyzing AUX1 gene expression in the acs11 mutant and ACS11 gene expression in the aux1 mutant. The GUS reporter lines ARR5::GUS, IAA2::GUS, and EBS::GUS were used to observe changes in cytokinin, auxin, and ethylene levels in the root, respectively. The results of this work suggest that cytokinin inhibits root cell elongation under B deficiency through two different mechanisms: (i) an ethylene-dependent mechanism through increased expression of the ACS11 gene, which would lead to increased ethylene in the root, and (ii) an ethylene-independent mechanism through decreased expression of the AUX1 gene, which alters auxin signaling in the meristematic and elongation zones and stele. We also report that changes in the expression of several B transporters occur in response to auxin, ethylene, and cytokinin that may affect the plant B content. Full article
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22 pages, 4052 KiB  
Article
Salt Pretreatment-Mediated Alleviation of Boron Toxicity in Safflower Cultivars: Growth, Boron Accumulation, Photochemical Activities, Antioxidant Defense Response
by Özlem Arslan, Şeküre Çulha Erdal and Yasemin Ekmekçi
Plants 2022, 11(17), 2316; https://doi.org/10.3390/plants11172316 - 04 Sep 2022
Cited by 1 | Viewed by 1677
Abstract
The study aims to elucidate alleviant effects of boron (B) toxicity by salt pretreatment (SP) on growth response, phytoremediation capacity, photosynthesis, and defense mechanisms in two safflower cultivars (Carthamus tinctorius L.; Dinçer and Remzibey-05). Eighteen-day-old plants were divided into two groups: SP [...] Read more.
The study aims to elucidate alleviant effects of boron (B) toxicity by salt pretreatment (SP) on growth response, phytoremediation capacity, photosynthesis, and defense mechanisms in two safflower cultivars (Carthamus tinctorius L.; Dinçer and Remzibey-05). Eighteen-day-old plants were divided into two groups: SP (75 mM NaCl for 5 days) and/or B treatment (C, 2, 4, 6, and 8 mM B for 10 days). Depending on the applied B toxicity, B concentrations in roots and leaves of both cultivars, necrotic areas of leaves, ion leakage (RLR), and H2O2 synthesis increased, while shoot and root length as well as biomass, water, chlorophyll a+b, and carotenoid content decreased. In addition, chlorophyll a fluorescence results revealed that every stage of the light reactions of photosynthesis was adversely affected under B toxicity, resulting in decreases in performance indexes (PIABS and PITOT). However, the cultivars tended to induce the synthesis of anthocyanins and flavonoids and increase the activity of antioxidant enzymes (SOD, POD, APX, and GR) to detoxify reactive oxygen species (ROS) under B toxicity. SP mitigated the negative effects of toxic B on biomass, water and pigment content, membrane integrity, photosynthetic activity, and defense systems. Considering all results, Remzibey-05 was able to better overcome the biochemical and physiological changes that may be caused by B toxicity by more effectively rendering B harmless, although it accumulated more B than Dinçer. Full article
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22 pages, 3030 KiB  
Article
Carbon-11 Radiotracing Reveals Physiological and Metabolic Responses of Maize Grown under Different Regimes of Boron Treatment
by Stacy L. Wilder, Stephanie Scott, Spenser Waller, Avery Powell, Mary Benoit, James M. Guthrie, Michael J. Schueller, Prameela Awale, Paula McSteen, Michaela S. Matthes and Richard A. Ferrieri
Plants 2022, 11(3), 241; https://doi.org/10.3390/plants11030241 - 18 Jan 2022
Cited by 5 | Viewed by 2009
Abstract
In agriculture, boron is known to play a critical role in healthy plant growth. To dissect the role of boron in maize metabolism, radioactive carbon-11 (t½ 20.4 min) was used to examine the physiological and metabolic responses of 3-week-old B73 maize plants [...] Read more.
In agriculture, boron is known to play a critical role in healthy plant growth. To dissect the role of boron in maize metabolism, radioactive carbon-11 (t½ 20.4 min) was used to examine the physiological and metabolic responses of 3-week-old B73 maize plants to different levels of boron spanning 0 mM, 0.05 mM, and 0.5 mM boric acid (BA) treatments. Growth behavior, of both shoots and roots, was recorded and correlated to plant physiological responses. 11CO2 fixation, leaf export of [11C]-photosynthates, and their rate of transport increased systematically with increasing BA concentrations, while the fraction of [11C]-photosynthates delivered to the roots under 0 mM and 0.5 mM BA treatments was lower than under 0.05 mM BA treatment, likely due to changes in root growth. Additionally, solid-phase extraction coupled with gamma counting, radio-fluorescence thin layer chromatography, and radio-fluorescence high-performance liquid chromatography techniques applied to tissue extracts provided insight into the effects of BA treatment on ‘new’ carbon (as 11C) metabolism. Most notable was the strong influence reducing boron levels had on raising 11C partitioning into glutamine, aspartic acid, and asparagine. Altogether, the growth of maize under different regimes of boron affected 11CO2 fixation, its metabolism and allocation belowground, and altered root growth. Finally, inductively coupled plasma mass spectrometry provided insight into the effects of BA treatment on plant uptake of other essential nutrients. Here, levels of boron and zinc systematically increased in foliar tissues with increasing BA concentration. However, levels of magnesium, potassium, calcium, manganese, and iron remained unaffected by treatment. The rise in foliar zinc levels with increased BA concentration may contribute to improved 11CO2 fixation under these conditions. Full article
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15 pages, 8288 KiB  
Article
One-Time Foliar Application and Continuous Resupply via Roots Equally Improved the Growth and Physiological Response of B-Deficient Oilseed Rape
by Anh Quang Dinh, Asif Naeem, Amit Sagervanshi and Karl H. Mühling
Plants 2021, 10(5), 866; https://doi.org/10.3390/plants10050866 - 26 Apr 2021
Cited by 3 | Viewed by 1902
Abstract
Oilseed rape (Brassica napus L.) is a high-boron (B)-demanding crop, and initially, normal growing plants might show B deficiency at advanced growth stages on soils with marginal B availability. Hence, we compared the effects of B resupply via roots and leaves on [...] Read more.
Oilseed rape (Brassica napus L.) is a high-boron (B)-demanding crop, and initially, normal growing plants might show B deficiency at advanced growth stages on soils with marginal B availability. Hence, we compared the effects of B resupply via roots and leaves on growth and physiological response, and relative expression of B transporters in B-deficient oilseed rape plants. Four-week-old plants initially grown with inadequate B (1 µM B for the first two weeks and 0.25 µM B for the next two weeks) were later grown either as such with 0.25 µM B, with 25 µM B in nutrient solution or foliar sprayed with 7 mL of 30, 60 and 150 mM B solution plant−1 as boric acid. Plants grown with 25 µM B in the nutrient solution from the beginning were included as adequate B treatment. Results showed that B resupply to B-deficient plants via roots and leaves (60 mM B) equally improved root and shoot dry matter, but not to the level of plants grown with adequate B supply. Foliar-applied 150 mM B proved toxic, causing leaf burn but not affecting dry matter. Resupply of B via roots increased B concentration in roots and leaves, while leaf-applied B did so only in leaves. Net carbon assimilation had a positive relationship with dry matter accumulation. Except for the highest foliar B level, B resupply via roots and leaves increased the accumulation of glucose, fructose and sucrose in leaves. Boron-deficient plants showed significant upregulation of BnaNIP5;1 in leaves and roots and of BnaBOR1;2 in roots. Boron resupply via roots reversed the B-deficiency-induced upregulation of BnaNIP5;1 in roots, whereas the expression of BnaBOR1;2 was reversed by both root and foliar B resupply. In leaves, B resupply by both methods reversed the expression of BnaNIP5;1 to the level of B-adequate plants. It is concluded that B resupply to B-deficient plants via roots and leaves equally but partially corrected B deficiency in B. napus grown in hydroponics. Full article
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Review

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25 pages, 1323 KiB  
Review
What Can Boron Deficiency Symptoms Tell Us about Its Function and Regulation?
by Luis Bolaños, Isidro Abreu, Ildefonso Bonilla, Juan J. Camacho-Cristóbal and María Reguera
Plants 2023, 12(4), 777; https://doi.org/10.3390/plants12040777 - 09 Feb 2023
Cited by 7 | Viewed by 3926
Abstract
On the eve of the 100th anniversary of Dr. Warington’s discovery of boron (B) as a nutrient essential for higher plants, “boronists” have struggled to demonstrate a role beyond its structural function in cell walls dimerizing pectin molecules of rhamnogalacturonan II [...] Read more.
On the eve of the 100th anniversary of Dr. Warington’s discovery of boron (B) as a nutrient essential for higher plants, “boronists” have struggled to demonstrate a role beyond its structural function in cell walls dimerizing pectin molecules of rhamnogalacturonan II (RGII). In this regard, B deficiency has been associated with a plethora of symptoms in plants that include macroscopic symptoms like growth arrest and cell death and biochemical or molecular symptoms that include changes in cell wall pore size, apoplast acidification, or a steep ROS production that leads to an oxidative burst. Aiming to shed light on B functions in plant biology, we proposed here a unifying model integrating the current knowledge about B function(s) in plants to explain why B deficiency can cause such remarkable effects on plant growth and development, impacting crop productivity. In addition, based on recent experimental evidence that suggests the existence of different B ligands other than RGII in plant cells, namely glycolipids, and glycoproteins, we proposed an experimental pipeline to identify putative missing ligands and to determine how they would integrate into the above-mentioned model. Full article
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13 pages, 1780 KiB  
Review
Citrus Physiological and Molecular Response to Boron Stresses
by Lin-Tong Yang, Jun-Feng Pan, Neng-Jing Hu, Huan-Huan Chen, Huan-Xin Jiang, Yi-Bin Lu and Li-Song Chen
Plants 2022, 11(1), 40; https://doi.org/10.3390/plants11010040 - 23 Dec 2021
Cited by 30 | Viewed by 4208
Abstract
Since the essentiality of boron (B) to plant growth was reported nearly one century ago, the implication of B in physiological performance, productivity and quality of agricultural products, and the morphogenesis of apical meristem in plants has widely been studied. B stresses (B [...] Read more.
Since the essentiality of boron (B) to plant growth was reported nearly one century ago, the implication of B in physiological performance, productivity and quality of agricultural products, and the morphogenesis of apical meristem in plants has widely been studied. B stresses (B deficiency and toxicity), which lead to atrophy of canopy and deterioration of Citrus fruits, have long been discovered in citrus orchards. This paper reviews the research progress of B stresses on Citrus growth, photosynthesis, light use efficiency, nutrient absorption, organic acid metabolism, sugar metabolism and relocation, and antioxidant system. Moreover, the beneficial effects of B on plant stress tolerance and further research in this area were also discussed. Full article
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