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Boron toxicity in higher plants: an update

DOI:10.1007/s00425-019-03220-4
Authors:
Marco Landi at Università di Pisa
Marco Landi
Theoni Margaritopoulou at Benaki Phytopathological Institute
Theoni Margaritopoulou
Ioannis E. Papadakis at Agricultural University of Athens
Ioannis E. Papadakis
Fabrizio Araniti at University of Milan
Fabrizio Araniti
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Abstract and Figures

Main conclusion In this review, emphasis is given to the most recent updates about morpho-anatomical, physiological, biochemical and molecular responses adopted by plants to cope with B excess. Abstract Boron (B) is a unique micronutrient for plants given that the range of B concentration from its essentiality to toxicity is extremely narrow, and also because it occurs as an uncharged molecule (boric acid) which can pass lipid bilayers without any degree of controls, as occurs for other ionic nutrients. Boron frequently exceeds the plant’s requirement in arid and semiarid environments due to poor drainage, and in agricultural soils close to coastal areas due to the intrusion of B-rich seawater in fresh aquifer or because of dispersion of seawater aerosol. Global releases of elemental B through weathering, volcanic and geothermal processes are also relevant in enriching B concentration in some areas. Considerable progress has been made in understanding how plants react to B toxicity and relevant efforts have been made to investigate: (I) B uptake and in planta partitioning, (II) physiological, biochemical, and molecular changes induced by B excess, with particular emphasis to the effects on the photosynthetic process, the B-triggered oxidative stress and responses of the antioxidant apparatus to B toxicity, and finally (III) mechanisms of B tolerance. Recent findings addressing the effects of B toxicity are reviewed here, intending to clarify the effect of B excess and to propose new perspectives aimed at driving future researches on the topic.
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Planta (2019) 250:1011–1032
https://doi.org/10.1007/s00425-019-03220-4
REVIEW
Boron toxicity inhigher plants: anupdate
MarcoLandi1· TheoniMargaritopoulou2· IoannisE.Papadakis3 · FabrizioAraniti4
Received: 27 March 2019 / Accepted: 18 June 2019 / Published online: 24 June 2019
© Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Main conclusion In this review, emphasis is given to the most recent updates about morpho-anatomical, physiologi-
cal, biochemical and molecular responses adopted by plants to cope with B excess.
Abstract Boron (B) is a unique micronutrient for plants given that the range of B concentration from its essentiality to
toxicity is extremely narrow, and also because it occurs as an uncharged molecule (boric acid) which can pass lipid bilayers
without any degree of controls, as occurs for other ionic nutrients. Boron frequently exceeds the plant’s requirement in arid
and semiarid environments due to poor drainage, and in agricultural soils close to coastal areas due to the intrusion of B-rich
seawater in fresh aquifer or because of dispersion of seawater aerosol. Global releases of elemental B through weathering,
volcanic and geothermal processes are also relevant in enriching B concentration in some areas. Considerable progress has
been made in understanding how plants react to B toxicity and relevant efforts have been made to investigate: (I) B uptake and
in planta partitioning, (II) physiological, biochemical, and molecular changes induced by B excess, with particular emphasis
to the effects on the photosynthetic process, the B-triggered oxidative stress and responses of the antioxidant apparatus to B
toxicity, and finally (III) mechanisms of B tolerance. Recent findings addressing the effects of B toxicity are reviewed here,
intending to clarify the effect of B excess and to propose new perspectives aimed at driving future researches on the topic.
Keywords Boric acid· Boron partitioning· Boron-polyol complexes· Boron tolerance· Boron transporter· Oxidative
stress
Introduction
Boron (B) toxicity limits crop yield and quality in several
agricultural areas worldwide, and frequently occurs naturally
in alkaline and saline soils together with a low rainfall and
very scarce leaching (Camacho-Cristóbal etal. 2018; Landi
etal. 2012), in agricultural lands close to coastal area (Kabay
etal. 2010) or in areas with persistent geothermal activities
(Princi etal. 2016a). Indeed, ocean evaporation is the pre-
dominant source of B release in the biosphere (65–85%),
whereas natural chemical and mechanical weathering of
sedimentary rocks provide B compounds in soil and water
(Princi etal. 2016a). The most impactful source of highly
concentrated B, with an average of 5–6mg B l−1 (Kabay
etal. 2010), is certainly the seawater, whose intrusion occurs
naturally in most coastal aquifers, owing to the hydraulic
connection between groundwater and seawater, thereby
increasing B concentration in irrigation water (Reid 2010).
Differently to other pollutants, environmental B release
that is directly or indirectly attributable to human activi-
ties plays a minor role compared to the amplitude of the
environmental B-enrichment deriving from natural sources.
List of anthropogenic sources based on their increased con-
tribution to B release worldwide is agriculture, wood burn-
ing, power generation from coal and oil, glass manufacture,
use of borates/perborates, borate mining and processing,
* Ioannis E. Papadakis
papadakis@aua.gr
1 Department ofAgriculture, Food andEnvironment,
University ofPisa, Via del Borghetto 80, 56124Pisa, Italy
2 Laboratory ofMycology, Department ofPhytopathology,
Benaki Phytopathological Institute, St. Delta 8,
14561Kifisia, Greece
3 Laboratory ofPomology, Department ofCrop Science,
Agricultural University ofAthens, Iera Odos 75,
11855Athens, Greece
4 Dipartimento AGRARIA, Università Mediterranea di Reggio
Calabria, Località Feo di Vito, SNC, 89124ReggioCalabria,
RC, Italy
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... The essentiality of this element was first reported in 1923 by Katherine Warrington who showed that the growth of Vicia faba (field bean) and other plants was reduced in the B deficiency, but it was rescued following the resupply of B (Warrington, 1923). Afterwards, it has been widely accepted that B is a necessary and beneficial element for different plants; the nutritional and physiological functions of B have been studied and reviewed elsewhere (Camacho-Cristóbal et al., 2018;Landi et al., 2019). Accordingly, B is an important element for cell wall formation and stability as well as the maintenance of plasma membrane functions (Brown et al., 2002). ...
... Moreover, B has been also associated with seed formation and development by directly impacting seed germination and seedling establishment (Zohaib et al., 2018). Notably, the influences of B on specialized metabolites biosynthesis such as antioxidants polyphenols has been also suggested since B nutrition is likely an important agent regulating reactive oxygen species (ROS) levels (Brown et al., 2002;Landi et al., 2019). B is also involved in RNA metabolism (pyrimidine biosynthesis) and indole-3-acetic acid oxidase root elongation (González-Fontes et al., 2015), phenolic metabolism, carbohydrate metabolism and translocation of photoassimilates (Graham and Webb, 1991); however, it is important to mention that the molecular mechanisms behind most of these functions remain largely unknown. ...
... In soil solution, B occurs mainly in the undissociated form of boric acid (H 3 BO 3 ), which greatly influences its availability (Brown et al., 2002). Generally, two extreme conditions, B deficiency and toxicity, are observed in arable lands drastically affecting crop production, yield, and quality, leading to significant economic losses (Camacho-Cristóbal et al., 2018;Landi et al., 2019). Noteworthy, studies on B fertilization have shown that the limits between deficiency and toxicity are very narrow and that the ideal dose is relatively variable across plant species (Camacho-Cristóbal et al., 2018;Landi et al., 2019). ...
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... Borax deficiency induces improper reproductive organ development and lowers plant output (Dell and Huang 1997;Chen et al. 2005;Nabi et al. 2006). Recently, from another perspective, B was assumed to be a rather toxic element, causing substantial damage to plant cells even at low levels (Reid et al. 2004;Landi et al. 2019). It is also necessary for blooming and fruit production (Nonnecke 1989). ...
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... High levels of B in the soil as well as in irrigation water, especially in dry and semi-arid region, impede plant development and reduce agricultural output and quality (Choudhary et al. 2020). B-toxic conditions occurs naturally in alkaline and saline soils as well as a low rainfall and very scarce leaching (Camacho-Cristóbal et al. 2008), in agricultural lands close to coastal area or in areas with persistent geothermal activities (Landi et al. 2019). Furthermore, B-toxic soils also occur as a consequence of over-fertilization and/or irrigation with water containing high levels of B (Camacho-Cristóbal et al. 2008). ...
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Arbuscular mycorrhizal symbiosis improves tolerance of Carrizo citrange to excess boron supply by reducing leaf B concentration and toxicity in the leaves and roots
Article
This study explores the possibility of using mycorrhization as a novel technique for diminishing the negative effects of boron (B) in the nutrient solution on seedlings of Carrizo citrange rootstock plants. For this, an experiment was planned for studying the physiological (gas exchange and chlorophyll fluorescence parameters), morphological (vegetative growth parameters), nutritional (organic solutes, carbohydrates) and oxidative stress responses of seedlings that were either mycorrhized (+AM, Rhizophagus irregularis; previously known as Glomus intraradices) or not mycorrhized (-AM), and irrigated with water containing different concentrations of B (0.5, 5 and 10 mg L −1). It was observed that an excess of B in the nutrient solution decreased the vegetative growth in both +AM and-AM plants, but this decrease was greater in-AM plants. Mycorrhized plants (+AM) under high B concentration accumulated less B in the leaves, and had a smaller reduction of net assimilation rate of CO 2 and lower MDA concentration than non-mycorrhized plants. Thus, it can be concluded that mycorrhization increased the tolerance to high boron concentration in the irrigation water of citrange Carrizo seedlings by reducing both the B concentration in the plant tissue and the B toxicity in the physiological processes. The study of organic solutes and carbohydrates also pointed to a different response model between +AM and-AM plants that could be related to the different tolerance observed between these plants.
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Boron and zinc deficiencies and toxicities and their interactions with other nutrients in soybean roots, leaves, and seeds
Article
  • Feb 2019
In many parts of the world, soils deficient and/or toxic in micronutrients reduce potential soybean (Glycine max) yields. The objective of our study was to grow plants in low to high concentrations of boron (B) and zinc (Zn) to determine how B and Zn deficiencies and toxicities affect soybean growth and interact with other essential nutrients in roots, leaves, and seeds. We found that B significantly affected levels of all essential nutrients except manganese and iron, while Zn significantly affected all essential nutrients in at least one plant tissue tested. Some of the physiological responses and nutrient interactions were cultivar-dependent. This study showed how deficiencies and toxicities of B and Zn affect plant growth and how B and Zn fertility interacts with many of the other essential nutrients.
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The Forner Alcaide nº 5 citrus genotype shows a different physiological response to the excess of boron in the irrigation water in relation to its two genotype progenitors
Article
Citrus rootstocks, (i.e. Carrizo citrange, Cleopatra mandarin, and Forner-Alcaide nº5) influence the agronomical and physiological behavior of citrus trees under unfavorable environmental conditions. Citrus are very sensitive to boron (B) toxicity. However, when good-quality water is scarce, growers must use water treatment and desalination plant water for irrigation, which may have a B concentration that is above the threshold recommended for citrus trees (0.5 mg L⁻¹). There is little information on the relative tolerance of citrus rootstocks to an excess of B, and the physiological and biochemical mechanisms involved. In this work, the morphological, physiological, biochemical and nutritional responses of three citrus rootstock plants, Carrizo citrange (Citrus sinensis (L.) Osb. × Poncirus trifoliata (L.) Raf.), Cleopatra mandarin (Citrus reshni Hort. ex Tan.) and Forner-Alcaide nº 5 (Cleopatra mandarin × Poncirus trifoliata (L.) Raf.), under different concentrations of B in the irrigation water (0.25, 5 and 10 mg L⁻¹), grown in containers in a greenhouse, were studied. The results showed that Carrizo citrange was very sensitive to B toxicity, as the plants had the most reduced vegetative growth, the greatest concentration of B in their leaves, stem and roots, a greater concentration of malondialdehyde in leaves, and a lesser net assimilation of CO2. The other two genotypes did not show differences in the accumulation of B in their tissues. Nevertheless, Cleopatra mandarin showed a greater tolerance, as its photosynthetic system was less affected by B toxicity, probably due to its potent antioxidant system, which is based on a high activity of catalase, which restricts the accumulation of malondialdehyde in its leaves. Forner-Alcaide nº 5 had an intermediate tolerance, similar to Cleopatra mandarin than to Carrizo citrange, as per the accumulation of B in its leaves. Forner-Alcaide nº 5 was the only genotype whose root was not affected by B toxicity.
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Changes in sugar metabolism associated to stem bark thickening partially assist young tissues of Eriobotrya japonica seedlings under boron stress
Article
Boron (B) toxicity frequently affects plant performances and productivity, especially in arid and semi-arid environments. In this experiment, loquat seedlings were subjected to 25 μM (control) or 400 μM B (B excess) to test the hypothesis that (i) B alters sugar/polyol metabolism in polyol-producing tree species as loquat and (ii) changes of leaf and stem anatomy assist young tissues against toxic effect of B. Gas exchange was monitored from the beginning of the experiment (FBE) till one week after the first visible symptoms of B toxicity appeared in the upper part of the stems (147 d FBE). At 147 FBE, plant biometric parameters and pattern of B accumulation, leaf and stem anatomy, chlorophyll a fluorescence kinetics as well as biochemical measurements were assessed in top (asymptomatic) leaves and upper stem bark. Boron accumulated principally (in the row) in top leaves > top bark > top wood in B-stressed plants, but no changes in allocation pattern were found between controls and B-stressed plants. Excess B promoted the increase in the spongy layer of top leaves and caused the development of cork and numerous collenchyma cells with increased cell wall thickness. This mechanism, which has never been described before, can be considered an attempt to store excessive B in tissues where B ions are less harmful. The accumulation of sorbitol (B-complexing polyol) in top leaves and stem bark can be considered as a further attempt to detoxify B excess. However, B toxicity drastically affects the photosynthetic rate of top leaves, mainly due to non-stomatal limitations, i.e., reduction of ambient CO2 use efficiency and of photosystem II (PSII) efficiency, modification of the partitioning excess energy dissipation in PSII, thus leading to an increased level of lipid peroxidation. Our results suggest that changes in sugar metabolism associated with leaf and stem bark thickening partially assist (but not totally preserve) young tissues of loquat plants under B stress.
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