Role of Boron and its Interaction with Other Elements in Plants PDF

TYPE Review PUBLISHED 12 February 2024 DOI 10.3389/fpls.2024...

TYPE Review PUBLISHED 12 February 2024 DOI 10.3389/fpls.2024.1332459 Role of boron and its interaction OPEN ACCESS with other elements in plants EDITED BY Saad Sulieman, Peter Vera-Maldonado 1, Felipe Aquea 2, Marjorie Reyes-Dı́az 3,4, University of Khartoum, Sudan REVIEWED BY Paz Cárcamo-Fincheira 3, Braulio Soto-Cerda 5,6, Jiashi Peng, Adriano Nunes-Nesi 7 and Claudio Inostroza-Blancheteau 5,6* Hunan University of Science and Technology, China 1 Programa de Doctorado en Ciencias Agropecuarias, Facultad de Recursos Naturales, Universidad Milka Brdar-Jokanović, Católica de Temuco, Temuco, Chile, 2 Laboratorio de Bioingenierı´a, Facultad de Ingenierı´a y Ciencias, Institute of Field and Vegetable Crops, Serbia Universidad Adolfo Ibáñez, Santiago, Chile, 3 Departamento de Ciencias Quı´micas y Recursos Naturales, Facultad de Ingenierı´a y Ciencias, Universidad de La Frontera, Temuco, Chile, 4 Center of *CORRESPONDENCE Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Claudio Inostroza-Blancheteau Nucleus (BIOREN), Universidad de La Frontera, Temuco, Chile, 5 Laboratorio de Fisiologı´a y [email protected] Biotecnologı´a Vegetal, Departamento de Ciencias Agropecuarias y Acuı´colas, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco, Chile, 6 Nucleo de Investigación en Producción RECEIVED 03 November 2023 Alimentaria, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco, Chile, ACCEPTED 03 January 2024 7 Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, MG, Brazil PUBLISHED 12 February 2024 CITATION Vera-Maldonado P, Aquea F, Reyes-Dı´az M, Cárcamo-Fincheira P, Soto-Cerda B, Boron (B) is an essential microelement for plants, and its deficiency can lead to Nunes-Nesi A and Inostroza-Blancheteau C impaired development and function. Around 50% of arable land in the world is (2024) Role of boron and its interaction with other elements in plants. acidic, and low pH in the soil solution decreases availability of several essential Front. Plant Sci. 15:1332459. mineral elements, including B, magnesium (Mg), calcium (Ca), and potassium (K). doi: 10.3389/fpls.2024.1332459 Plants take up soil B in the form of boric acid (H3BO3) in acidic soil or tetrahydroxy COPYRIGHT borate [B(OH)4]- at neutral or alkaline pH. Boron can participate directly or © 2024 Vera-Maldonado, Aquea, Reyes-Dı´az, Cárcamo-Fincheira, Soto-Cerda, Nunes-Nesi indirectly in plant metabolism, including in the synthesis of the cell wall and and Inostroza-Blancheteau. This is an open- plasma membrane, in carbohydrate and protein metabolism, and in the access article distributed under the terms of formation of ribonucleic acid (RNA). In addition, B interacts with other the Creative Commons Attribution License (CC BY). The use, distribution or reproduction nutrients such as Ca, nitrogen (N), phosphorus (P), K, and zinc (Zn). In this in other forums is permitted, provided the review, we discuss the mechanisms of B uptake, translocation, and original author(s) and the copyright owner(s) are credited and that the original publication accumulation and its interactions with other elements, and how it contributes in this journal is cited, in accordance with to the adaptation of plants to different environmental conditions. We also discuss accepted academic practice. No use, potential B-mediated networks at the physiological and molecular levels involved distribution or reproduction is permitted which does not comply with these terms. in plant growth and development. KEYWORDS boron, interaction, mineral elements, low pH, protein transport, oxidative stress Introduction Boron (B) is an essential element for growth, development, productivity and quality of crops (Wang et al., 2015; Shireen et al., 2018; Pereira et al., 2021). It is found in soils as boric acid [B(OH)3] and tetrahydroxy borate [B(OH)4]-, and is distributed unevenly in soil solution and in organic and mineral fractions depending on the soil pH (Hrmova et al., 2020). Boron is considered as the most mobile, and often one of the most deficient, microelements in soils (Wimmer and Eichert, 2013; Hrmova et al., 2020). Plant absorbs B as [B(OH)3] via the channels in the plasma membrane, and export [B(OH)4]- through specific transporters (Stangoulis et al., 2001; Yoshinari and Takano, 2017). The availability Frontiers in Plant Science 01 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 of B in soils depends on adsorption-desorption processes, which are particular, B interactions (synergistic or antagonistic) can affect influenced by various physicochemical characteristics such as soil plant nutrition, but the effects of deficient or excessive supply of B pH, texture, moisture, clay content and type of clay minerals, on mineral uptake and functions are not well established. hydroxy-oxides of aluminum (Al) and iron (Fe), calcium There are contrasting results concerning mineral uptake, carbonate (CaCO3), and organic matter (Arora and Chahal, potentially due to the use of many crop species (Lombin and 2010). A positive correlation has been reported between B Bates, 1982), as well as varieties (Mozafar, 1989). Similarly, the adsorption on clay minerals or Al hydroxy-oxides and soil pH use of nutrient solution (Wallace et al., 1977) or diverse soils types (Keren, 1996). At pH below 7.0, the dominant B form [B(OH)3] (Singh and Sinha, 1976; Agbenin et al., 1991), and the shows relatively low affinity for clay, but in the alkaline pH range, characterization s of different plant parts (Miller and Smith, 1977; the proportion of borate increases rapidly, reaching maximum Singh and Singh, 1984) at various growth stages (Carpena-Artes adsorption around pH 9.0 (Elrashidi and O’Connor, 1982). and Carpena-Ruiz, 1987) might have contributed to such Boron is a microelement and its concentration in dried leaf tissue apparently inconsistent findings. The present review is aimed at varies depending on species and genotypes (Arunkumar et al., 2018). critically appraising the available information on the interaction Boron participates in cell wall biosynthesis and structural integrity between B and other mineral elements, based on the hypothesis that (Shireen et al., 2018; Pereira et al., 2021), mainly related to the B (being involved in many physiological and biochemical processes) formation of borate esters with rhamnogalacturonan (RG‐II) that influences uptake and utilization of other plant nutrients and improve the porosity and elasticity of the cell wall (Funakawa and beneficial elements. We critically discuss the current knowledge Miwa, 2015; Nejad and Etesami, 2020). In Arabidopsis thaliana roots, about the role of B and its physiological and molecular relationships B is essential for the crosslinking of cell wall RG-II and pectin with other elements, with the aim of laying the groundwork for the assembly (Camacho-Cristó bal et al., 2008). In addition, it is also identification of relevant interaction networks involved in plant involved in the stimulation of reproductive tissues, improvement of growth and development. seed quality, ion traffic through the membranes, cell division and elongation, protein cytoskeletal function, the metabolism of antioxidants, ascorbic acid and polyphenols, sugar transport, Interaction of B and macroelements oxidoreductase activity, and the biosynthesis and transport of plant hormones, among other processes (Lu et al., 2015; Shireen et al., 2018). Boron interactions with nitrogen By comparing the B concentrations in plants, it has been observed, for example, that an optimal B concentration enhances Nitrogen (N) in plants enhances vegetative growth, H+-ATPase activity, thus maintaining the electrochemical gradients photosynthetic rates, chlorophyll content, and is an essential across the plasma membrane; by contrast, under limited availability mineral nutrient for plant growth and development (Sakuraba, of B, reduced H+-ATPase activity is found in plasma membrane- 2022). Nitrogen is a component of proteins, amino acids, enriched vesicles isolated from Cicer arietinum roots (Shireen et al., nucleotides, and nucleic acids (Koohkan and Maftoun, 2016). 2018). Under B deficiency, an excessive accumulation of soluble Regarding the interaction with B, it has been shown that B is sugars has been observed in the plant leaves by a reduction in the related to N assimilation in plants (Long and Peng, 2023). photosynthates translocation (Camacho-Cristó bal et al., 2004). This Furthermore, the interaction of B and N has great importance could affect increasing the concentration of phenolic compounds because of the interference of N in B nutrition, either promoting or and others derivatives, like quinones, which may be oxidized and reducing the absorption of B in plants (Petridis et al., 2013). In Vicia exacerbate reactive oxygen species (ROS) production, including faba L. (faba bean), the interaction between B and N affects the oxygen radicals (Han et al., 2008). absorption and utilization of N and other nutrients, such as P, K, Two functionallly different kinds of transporters have been Ca, and Mg, influencing plant growth in terms of height, leaf area, identified in plant cells: boron transporters (BORs) that have a B number of pods, and seed yield (Mahmoud et al., 2006) (Table 1). In export function in plant cells, and nodulin-26-like intrinsic protein Brassica napus L. (canola), N application in conditions of excess B (NIPs) members of the major intrinsic proteins (MIP) family, that improve the chlorophyll levels and decrease the severity of B include some boric acid channels (Wang et al., 2015; Zhang et al. toxicity symptoms (Koohkan and Maftoun, 2016). Recently, the 2022; Pereira et al., 2021). BOR1 was first reported in A. thaliana effects of the B x N interaction on winter triticale (x Triticosecale and is necessary for effective transport in the xylem, preferentially Wittmack) productivity have been reported, whereby the for the translocation of B into younger parts of plants (Takano et al., application of B increases grain yield and improves the yield 2001; Takano et al., 2002). Additionally, aquaporins in the NIP components, mainly the number of ears (Bielski et al., 2020). subgroup have been identified as boric acid channels required for Boron has also been shown to be essential in N2 fixation and plant growth under B deficiency. The NIP5;1 transporter gene is assimilation regarding nodulation in soybean (Glycine max) expressed in plasma membrane of root epidermis cortical and (Table 1) due to the impaired biosynthesis of early nodullin endodermal cells for boric acid transported, whereas the boric proteins (ENOD2) and malfunction of the oxygen diffusion acid channel NIP6;1 is involved in the B transport for barrier when B is scarce (Bellaloui et al., 2014). Boron deficiency proliferative plant tissues (Zhou et al., 2015). in the culture medium supporting peas (Pisum sativum L.) Boron interacts with other mineral elements, influencing several diminishes symbiotic N2 fixation by reducing the number of physiological and biochemical processes (Tariq and Mott, 2007). In nodules and interfering with their development, as well as causing Frontiers in Plant Science 02 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 TABLE 1 Interaction of boron with other minerals in different plant species. Plant Deficiency effect of Minerals Function Response Synergism Reference species an element Cell wall biosynthesis, Both influence the functions of + sugar transport, cell walls, allowing better + carbohydrate and RNA mobility in the plant metabolism Tomato Low B level provoked abnormal At the foliar level, it promotes (Ş ahin et al., 2015) B - Ca Vegetative and Peppers changes in the cell wall plant development and increases (Zeist et al., 2018) productive fruit production in pepper plants development of fruits and vegetables Boron deficiency disrupts Al- The entry of Al prevents the – induced inhibition of root solubility of B, inhibiting the (Li et al., 2018). Decreases toxicity Pea, B - Al elongation by accumulation of Al production of roots (Yan et al., 2019) of Al Orange in the transition zone of (Yan et al., 2022) lateral roots Boron deficiency causes a drastic B improves nitrate levels + (Bellaloui et al., decrease in nitrate content and B in rhizobial N fixation, + 2012) (Mahmoud Fixation of N nitrate reductase activity, and actinomycete symbiosis and et al., 2006) (formation of nodules) increases the content of formation of cyanophyte (Cervilla et al., Promotes the Soybean B-N carbohydrates in leaves from heterocysts in legume crops 2009) absorption and Tobacco tobacco plants Additively increases the content (Camacho- utilization of N and of nutrients in plant tissues Cristó bal and other nutrients Gonzalez- Fontes, 1999) Boron deficiency reduces Both are involved in the + (Petridis et al., phosphate absorption capacity, functions of the plasma 2013) Lettuce due to reductase activity membrane, influencing Tariq and Mott, Sugars and Rice B-P cell growth 2007) cell divisió n Corn (Atique-ur- and beans Rehman et al., 2018) Boron deficiency decreases The contribution of both + permeability to K at the improves the production of + cell membrane grains and leaves Buffers and improves With an optimal level of B, the (Rehim et al., cell membrane permeability of K in the cell Corn 2018) permeability and membrane increases B-K Sunflower (Samet et al., 2015) protein synthesis Both help to maintain conductive Cotton (Azeem Vegetative and tissues and to exert a regulatory et al., 2020) reproductive growth effect on other elements Foliar application of both increases biomass production and cotton yield Zn deficiency reduces the activity Between the two, they influence + Pollination, seed of RNA polymerase pollination and seed formation + (Ziaeyan and formation. Boron deficiency decreases Zn B increases growth and Corn Rajaie, 2009) Intervenes in RNA uptake in the plant chlorophyll content B - Zn Rice (Tariq and Mott, processes The lack of B decreases growth Pistachio 2007) Structural role in the and photosynthesis parameters (Tavallali, 2017) cell wall Zinc deficiency reduces stomatal conductance disorganization and changes in the cell wall structure (Ahmad effective in improving the nutritional status, since it increases the et al., 2009). concentration of N, P and K in the leaf, as well as the levels of Studies performed in canola (Brassica napus L.) show negative chlorophylls and carbohydrates, and the C/N ratio (Shaban effects of excess B on plant yield, which could be alleviated with N et al., 2019). fertilization (Koohkan and Maftoun, 2016). This result suggests that An important feature of the B x N interaction is the high N might alleviate the growth suppression effects caused by B mobility that both elements possess in soil (Brown and Shelp, 1997; toxicity, due to the formers positive effects on chlorophyll levels Grohskopf et al., 2020). Several studies suggest that N supply in and photosynthesis in canola (Brassica napus L.) plants (Koohkan different concentrations leads to a decrease in B uptake by the and Maftoun, 2016). Nonetheless, other research groups reporte plants. Nevertheless, the reported results regarding the effect of N that the foliar application of B in mango (Mangifera indica L.) was on B deficiency are still controversial and need further investigation Frontiers in Plant Science 03 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 (Lou et al., 2003). Thus, at the present time, several studies indicate period of B deficiency, therefore, it cannot be ruled out that the the presence of many gaps in our knowledge that remain to be changes in gene regulation are an indirect effect due to poor cellular elucidated in the B x N interaction. development of the plants. Also, enzymes such as glutamine Likewise, molecular mechanisms, pathways and interactions are synthetase and asparagine synthetase, increased transcript levels still a subject that needs deeper study, as most studies have focused subjected to B depleted conditions (Beato et al., 2010; Beato et al., on the improvement and alleviation of B stress at a physiological 2014), even though these genes could be considered as general level (Seeda et al., 2021; Long and Peng, 2023). Nevertheless, as new responsive genes activated under various abiotic stresses. Another molecular biology techniques arise together with bioinformatics, it important feature of this interaction at a molecular level is a study becomes increasingly interesting to try and elucidate the interaction carried out by Camacho-Cristó bal and Gonzá lez-Fontes (2007), of B with different elements at a molecular level. Thus, it has been where they found that short-term B deficiency decreases nitrate reported that B deficiency affects the transcriptional level of genes content in leaves of tobacco plants, possibly due to a drop in the related to nitrate assimilation (Camacho-Cristó bal et al., 2011; levels of H+-ATPase (PMA2) plasma membrane transcripts. Beato et al., 2014). For example, in root the mRNA concentration Nonetheless, these findings need to be further investigated. of NRT2 (High Affinity Nitrate Transporter) and leaf NIA (Nitrate Reductase) genes are low in tobacco (Nicotina tabacum) plants subjected to severe B deficiency, compared to control samples Boron interaction with phosphorus (Camacho-Cristó bal and Gonzalez-Fontes, 1999; Camacho- Cristó bal and Gonzalez-Fontes, 2007) (Table 2). Nonetheless, Phosphorus (P) is an essential macronutrient for plant growth have in mind that these studies were subjected to a long-term and productivity. This element is a key constituent of TABLE 2 Molecular interaction of boron with other minerals in different plant species. Minerals Plant Genes Response Reference B-N Tobacco NtNRT2 (high affinity Boron can regulate positive or negative nitrate transporters (Camacho-Cristó bal and nitrate transporter) Gonzalez-Fontes, 2007) NtNIA (nitrate reductase) B-P Rapeseed BnaPT10, BnaPT11, B could have a role in regulating the expression of P transport genes in (Li et al. 2019a; Hua et al., 2017) BnaPT35 and BnaPT3 roots under low P conditions (Zhao et al., 2020) BnaPHT1 High supply of B induces the expression of P-starvation BnaC3, SPX3 and BnaC3, SPX3 the P-transport genes in roots under low P availability. B-K Arabidopsis AtAGP13 B regulate the expression of AGP genes under B deficiency (Armengaud et al., 2004) B - Ca Arabidopsis AtCNGC19; AtACA; Low B may regulate the expression of CNGC19, ACA and CAX3 Ca2+ (Quiles-Pando et al., 2013) AtCAX, transporter genes and induce an augmented in the cytosolic Ca2+, also, it (Quiles-Pando et al., 2019) AtCNGC19, AtACA could be attributed to the expression of Ca2+ transporters, regulating Ca2+ and AtCAX homeostasis in B deficiency. B - Zn Arabidopsis At1g03770 B could regulate the expression of the At1g03770 gene that is predicted to (Kasajima and Fujiwara, 2007) Barley HvC2H2 encode transcription factors of the zinc finger family, involved in the (Pandey et al., 2022) downstream regulation of genes in response to high B levels. B could regulate the expression of C2H2 under toxic B conditions B - Si Rice OsLsi1 (NIP III); NIP members have been shown to be involved in the uptake of B and Si (Shao et al., 2018) Barley HvLsi1/HvNIP2;1 (Schnurbusch et al., 2010) B - Al Citrus XP_006479398 Gen expression in Citrus grandis roots showed that B appears to alleviate (Zhou et al., 2015) (Flavonol synthase/ Al toxicity (Yang et al., 2018) flavanone 3- Alleviation of B-induced Al toxicity; Regulation of the ABC transporter hydroxylase-like), NP_197540 (Flavanone 3 hydroxylase-like); ADL36732 (HSF domain class transcription factor) ATP Binding Cassette (ABC) B - Cd Rice OsHMA2, OsHMA3, Boron inhibits the expression of these Cd transporters, reducing Cd uptake (Qin et al. 2022) and OsNramp1, and transport, decreasing Cd accumulation in aboveground and (Riaz et al., 2020; Riaz et al., OsHMA2, Nramp1, belowground parts of rice plants. 2021) and ABC (Huang et al., 2021) Frontiers in Plant Science 04 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 macromolecules like nucleic acids, nucleotides and phospholipids of in B. napus plants (Hua et al., 2017). In a more up-to-date study in the plasma membrane. Phosphorus is also involved in several this species, the authors suggest that a high supply of B could induce biological processes such as protein regulation, photosynthesis, the expression of the P-starvation-induced gene BnaC3.SPX3 (SPX- cell division, respiration, and of coenzymes that activate synthesis domain-containing proteins) and the P-transport genes in roots of amino acids and other compounds (Vance et al., 2003; Paz-Ares under low P conditions (Zhao et al., 2020). In spite of these findings, et al., 2022) (Table 1). The interaction of B x P is not yet clear; the molecular interaccion between B and P transport remains nonetheless, borates and phosphates are similar in their action in poorly understood. several physiological and biochemical aspects. For example, both borates and phosphates form physiologically active esters with organic compounds due to their polyhydroxy nature (Atique-ur- Boron interaction with potassium Rehman et al., 2018). The uptake and transport of B in plants has been associated with P uptake, because when the concentration of B Potassium (K) is an essential macronutrient for plants, key in is low, phosphate uptake decreases, which then recovers when B is several metabolic processes, such as enzyme activation, stomata supplied (Table 1) (Atique-ur-Rehman et al., 2018). A recent study regulation, balance in the change of anions, and physiological suggests that B supply modulates H+-ATPase-mediated plasma function in plant cell, among others (Fageira, 2001). Nonetheless, membrane nutrient uptake in three species of Citrus [C. sinensis little research has been carried out on the interaction between B and (L.) Osbeck cv. Valencia, C. limonia (L.) Osbeck, and C. paradisi K in plants. Studies performed in B. napus show a positive correlation Macf. X Ponsirus trifoliata (L.) Raf.] (Ferreira et al., 2020). In this between B x K interactions, due to a significant increase in seed oil sense, B could be related to a reduction in the absorption capacity of content and overall oil yield in this crop (Chen et al., 1997). Another phosphate due to the decay of the ATPase activity (Yan et al., 2002). study conducted by Liza et al. (2021) reveals that the combined Furthermore, it has been reported that the synergistic effect nutrition of B and K results in a significant increase in growth, as well between B and P modulates the absorption and distribution of P, as as a 40% rise in yield compared to when the nutrients were provided well as the improvement of the photosynthetic rate and growth in B. individually to mung beans (Vigna radiata L.). In this context, the napus plants (Zhao et al., 2020). Another example is the foliar authors suggest that whilst K promotes a higher photosynthetic rate, application of B in jojoba plants [Simmondsia chinensis (Link) B participates in cell division and cell elongation, so their interaction Schneider], where the P level in leaves increases, and where both results in improved plant growth. Similar results were reported by elements show a significant response in improving plant growth, Azeem et al. (2020), where the combined leaf application of B + K yield and seed quality under desert conditions (Khattab et al., 2019). fertilization has a positive impact on growth and yield of cotton In addition, P nutrition mitigates the adverse effects of B toxicity on (Gossypium hirsutum L.). This treatment increases biomass yield and fruit growth in tomato (Solanum lycopersicum L.) plants production as well as vegetative and reproductive activity under (Kaya et al., 2009). In this sense, it has been described that P can high salinity conditions (Table 1). These results could be related to reduce the harmful effects of B toxicity on plant growth and the role of K in osmotic processes, carbohydrate and protein performance through the reduction of B absorption in tomato biosynthesis, the closing of stomata, membrane permeability and (Nejad and Etesami, 2020). pH control in plants (Ragel et al. 2019). On the other hand, Zhao et al. (2021a) show that the application Other studies show that B application increases B and K of B and P displays a synergistic and positive response, by increasing concentrations in rice (O. sativa L.), given that B doses increase K seed yield and phosphorus use efficiency (PUE). Also, sequencing of permeability in the plasma membrane of the cell (Atique-ur- 16S rRNA genes of bacterial community, reveal that the treatment Rehman et al. 2018). In fact, it is known that B influences the of B and P increased the diversity of soil bacteria in B. napus plants. activation of the cell membrane through H+-ATPase activity in root Furthermore, the effect of Bacillus pumilus bacteria on the cells, as H+ pumping drives hyperpolarization of the plasma absorption of B and P after application of both elements membrane, thus triggering K uptake to maintain electrochemical improves growth in B. napus plants compared with the control balance at the cellular level (Mattos et al., 2017). In tomato plants, (Masood et al., 2019). Moreover, the inoculation of B. pumilus Kaya and Ashraf (2015) describe that B toxicity significantly improves B levels in B. napus plants in B-deficient soils. However, reduces K availability in leaves, as well as that of N and Ca, whilst the dicovery of these interactions with biotic and abiotic factors are foliar application of nitric oxide decreases B concentration and recent and require further studies to fully understand their effects augments K, N, and Ca in tomato leaves. In addition, a study on different species. focused on the B x K interaction in wheat (T. aestivum L.) reports At the molecular level, little it known about the interaction that B toxicity significantly decreases the concentration of K in between B x P; however it has been documented that B could play a shoots (El-Shazoly et al., 2019). role in regulating the expression of P transport genes in roots of B. The B x K interaction at the molecular level has not been napus under low P conditions. Several genes have been identified studied exhaustively. A gene expression study using microarrays in such as BnaPT10, BnaPT11, BnaPT35 and BnaPT3, that tend to be A. thaliana reports that genes like AGP13, AGP14, and AGP22, are simultaneously induced by both P and B deficiencies (Hua et al., downregulated under B deficiency (Camacho-Cristó bal et al., 2008). 2017; Li et al., 2019a) (Table 2). These BnaPHT1 genes are poorly Interestingly, AGP13 (arabinogalactans, AGP) transcripts are also induced by B and have been detected in B-deficiency transcriptomes downregulated in A. thaliana roots during K starvation, even in the Frontiers in Plant Science 05 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 absence of fluctuating B levels (Armengaud et al., 2004) (Table 2). and ascorbate peroxidase (Siddiqui et al., 2012). Similar results have AGPs are proteins that are distributed differently throughout plant been reported by Liu et al. (2019), where Ca reduces B toxicity in tissues depending on their development, and these may be possible trifoliate rootstocks (Poncirus trifoliate L) by maintaining the candidates at a cell surface level like signaling across the cell wall, antioxidant enzyme system, and diminishing B concentration in plasma membrane and cytoskeleton (Sardar et al., 2006; Pereira the cell wall and intracellularly. Together, these results suggest that et al., 2014). In this sense, changes in B concentrations may Ca nutrition can be recommended as an agronomic management activated a cascade of signals, which may extend through practice strategy that mitigates B toxicity. cytoplasm, cell wall, plasma membrane, and cytoskeleton like a In durum wheat (Triticum durum L.), and bread wheat continuum, with the possible involvement of such proteins (Triticum aestivum L.) genotypes, an assay in plant pots was (Goldbach and Wimmer, 2007). carried out to evaluate the effects of B application on Ca, showing that high doses of B enhance the concentration and overall quantity of B in leaf cell walls, whereas a fall in cell wall Ca concentration is Boron interaction with calcium observed (Turan et al., 2018). This suggests that a negative interaction between Ca x B could decrease B excess in wheat and The B x Ca relationship has been observed mainly through the other related plant species. Nevertheless, further cellular research is cross-linking of pectin polysaccharides in the plant cell wall required to assess the affinity of Ca and B with respect to (Kobayashi et al., 1999); however, the nature of this interaction is crosslinking within the cell wall. In this context, several reports still debated. Several reports suggest a role for Ca in the stabilization have shown that these two elements, B and Ca, are closely related to of B complexes (B-RG-II), specifically in its ability to bind to each other; consequently, the deficiency or excess of B or Ca can carboxyl groups of the polygalacturonic acid regions (Kobayashi affect the nutritional status of the other, and even of other elements et al., 1999; Chormova et al., 2014b; Liu et al., 2019). In fact, a close (Krug et al., 2009; Gonzá lez-Fontes et al. 2014; Piñero et al., 2017). relationship between B x Ca with respect to cell wall functionality Therefore, B and Ca are crucial for plant performance and influence and integrity has been reported, where Ca plays a fundamental role the firmness and quality of seeds and fruits, and consequently it in wall plasticity and elongation, and B is involved in wall becomes necessary to understand and deepen our knowledge of the metabolism through the maintenance of the Ca-pectin interactions of these nutrients at a physiological, biochemical and association, influencing the development of the cell wall molecular level. (Yamauchi et al., 1986). Accordingly, it has been reported that in As stated, B deficiency also affects the expression of genes vitro dimerization of pectins such as RG-II are slow, but rise involved in major physiological processes. However, the signal markedly when Ca is applied, as shown in rose (Rosa sp) cells in transduction pathways through which plants are able to sense and B-free medium (Chormova et al., 2014b). In addition, several transmit B-deprivation signals to the nucleus are unknown. studies have presented evidence that Ca2+ is a constituent for the Consequently, a study investigated whether short-term B formation of borate-RG II complexes, stabilizing the pectic deficiency in A. thaliana roots affects cytosolic Ca levels and polysaccharides in the cell wall (Kobayashi et al., 1999; Goldbach signaling. The authors suggest that B deficiency induced an early et al., 2007; Chormova et al., 2014a; Li et al., 2017). Studies response of genes such as CNGC19 Ca2+-influx channel, ACA- and performed in pea under salt stress conditions show that the CAX-efflux, and Ca 2+ sensor genes, which regulate Ca 2+ addition of B and Ca positively affect root elongation and plant homeostasis (Quiles-Pando et al., 2013). This suggests that gene development (El-Hamdaoui et al., 2003). It has also been observed regulation under B deficiency could enhance the ability to transport that the N content in plants originating from seeds is decreased by Ca2+ from the cytosol to plastids, apoplasts, and vacuoles and thus salt stress and enhanced by B and Ca supply (Bonilla et al., 2004), restore cytosolic Ca2+ homeostasis (Table 2). On the other hand, suggesting an important role of B and Ca in the remobilization of Gonzá lez-Fontes et al. (2014) reported that at short-term, B nutrients stored in seed. On the other hand, experiments carried out deficiency affects cytosolic Ca2+ levels, and in roots, upregulates in pansy (Viola xwittrockiana Gams.), petunia (Petunia xhybrida the expression of genes from the MYB protein family involved in hort. Vilm.), and gerbera daisy (Gerbera jamesonii Bol. ex Adlam.) Ca2+ signaling and represses genes of the bZIP protein family with show that plants in the absence of Ca or B exhibit discoloration roles as channels/transporters, sensor relays and responders that act (chlorosis) and upward rolling of leaves, as well as thickening of as intermediaries in a transduction pathway triggered by B leaves, distorted meristems, and strap-like leaves, leading ultimately deficiency, with important consequences in plant development, to necrosis (Krug et al., 2009). The authors show that a temporary growth, flower maturation and stress (Zhao et al., 2021b). deficiency of either Ca or B provokes lasting symptoms throughout Another study performed in tobacco plants shows that short-term the whole production cycle, although the symptoms were more B deficiency is related with the influx of Ca2+ ions and the similar to those caused by B deficiency than to those that arise due expression of WIPK and WIZZ, associated with BY-2 cells and to a lack of Ca. Other studies in radish plants (Raphanus sativus L.) pectin network structure (Koshiba et al., 2009). A more recent study report the effect of supplying Ca in ameliorating B toxicity. Indeed, by Quiles-Pando et al. (2019), supports the idea that B deficiency Ca reduces the accumulation of B, and mitigates cellular oxidative regulates the expression of Ca2+ transporter genes such as CNGC19, damage by enhancing the antioxidant activity of enzymes like ACA and CAX3, triggering an increase in the Ca2+ concentration in superoxide dismutase, catalase, peroxidase, glutathione reductase, the cytoplasm. This might be attributed to the expression of Ca2+ Frontiers in Plant Science 06 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 transporters in an attempt to regulate Ca2+ homeostasis based on a hand, as mentioned above, B and Zn are important microelements response due to B deficiency. for normal plant function (Shrestha et al., 2020; Meriño- Gergichevich et al., 2021; Verma et al., 2021). However, even though their effects have long been investigated in many Interaction of B and microelements agronomical and molecular studies, the interaction of B x Zn remains scarce knowledge at genomic and transcriptomic levels. Boron interaction with zinc At a proteomic level, the differential expression of HKX1 and MAKR6 genes using the RAPD-PCR method in strawberry plants The interaction between different nutritional elements is very exposed to combined doses of B x Zn (Kiryakova et al., 2016) was important in plant nutrition. The B x Zn interaction affects analyzed. The function of the proteins encoded by these genes is metabolic processes in whole plant either stimulating or mainly related to plant hormones, signal transduction and sugar inhibiting the uptake of other nutrients hence, effecting the metabolism (Jing et al., 2020; Novikova et al., 2022), raising interest mineral composition In calcareous soils, Hosseini et al. (2007) in such genes whose expression may offer protection during the B x studied the B x Zn interaction in maize plants (Zea mays L.), Zn interaction. In another study at the proteomic level, under low discovering that Zn significantly increases plant height and dry and high B conditions in A. thaliana, RING1B was reportedly matter yield, whereas high B levels reduce plant height and dry induced by high B content in roots, with a locus tag At1g03770 matter yield, suggesting that the B x Zn interaction was antagonistic (Kasajima and Fujiwara, 2007). RING1B is predicted to encode a Zn on nutrient concentration and synergistic on plant growth. In this finger family transcription factor, and therefore it is possible that case, agronomically it is recommended to add Zn supplements in this gene regulates the expression of genes that are highly- soils with high B levels, particularly when Zn availability in soil is responsive to B. Besides, RING1B has been classified with an low. In maize, B and Zn fertilization produce significant changes in important role in the maintenance of shoot stem cell activity some plant nutrients, although these differences were marginal and (Chen et al., 2010). did not affect plant growth and production (Hosseini et al., 2007). Another example is the gene encoding a C2H2 Zn finger Another study carried out by Tavallali (2017) describes the effects of transcription factor protein which shows a two-fold upregulation in Zn and B on physiological and biochemical aspects in pistachio barley plants under B-toxic conditions (Pandey et al., 2022) (See plants (Pistacia vera L. cv. Badami). This study suggests that high B Table 2). This particular gene has been shown to be involved in plant levels, as well as the lack of B, could reduce growth and growth and development, stress signal transduction and, more photosynthetic parameters (Table 1), particularly under low Zn particularly, responses to abiotic stress (Han et al., 2020). levels. These authors report that Zn deficiency results in a reduction Nevertheless, its expression is not upregulated enough to be highly in net photosynthesis (Pn) and stomatal conductance (gs). significant. A more up-to-date RNA-seq study shows an important Nonetheless, the adverse effects of low and high B levels are enrichment of three genes of the C3H gene family (123068901, mitigated by increasing Zn concentration up to 10 mg kg−1 soil. 123060371 and 123189473), which belong to a subgroup of the In fruit species, B and Zn are important elements for normal fruit family of Zinc Finger Proteins and are observed under high B growth and development, whose deficiency affects metabolic conditions in wheat Triticum dicoccum shoots (Khan et al., 2023). processes, such as reduced shoot growth, mineral and nutritional alteration, and fruit quality (Marschner, 2012; Özenç and Özenç, 2015; Davarpanah et al., 2016). Foliar application of B and Zn in Boron interaction with manganese different doses in European hazelnut (Corylus avellana) show that only Zn significantly increases in kernels, and also leads to rises in Manganese (Mn) is an important element for plant growth and Ca and Na concentration in leaves (Meriño-Gergichevich et al., development (Li et al. 2019a). It acts as a cofactor in enzymatic 2021). The authors conclude that the foliar application of B and Zn activity, and of the oxygen-evolving complex (OEC) in the (at 800 and 400 mg L-1 respectively) are the most efficient doses for photosynthetic machinery in the catalysis of the water-splitting boosting the yield of fruits per plant. On the other hand, in olive reaction in photosystem II (PSII) (Alejandro et al., 2020). Other cultivars (Olea europea L.), foliar application of B and Zn increases functions of Mn are associated with the control of the biosynthesis phenolic compounds and oil content during the fruit ripening of the phenolic polymers lignin and suberin, compounds related to process (Saadati et al., 2013). The oil content increases from the resistance of enzymatic degradation, and avoidance of fungal 11.7% to 19.4%, highlighting that the applications of B and Zn pathogen invasion in plants (Vidhyasekaran, 2004; Agrios, 2005; improve the ratio of unsaturated/saturated fatty acids with respect Simoglou and Dordas, 2006). In this sense, a work that combined B, to the control plants. Moreover, in a soil experiment Quddus et al. Zn and Mn nutrition in coffee (Coffea arabica L.) plants showed that (2022) show that different doses of B (0, 1, 2 and 3 kg ha-1) and Zn all three elements affect the polyphenol concentration, but only Mn (0, 2, 3 and 4 kg ha-1) affect nutrient absorption, yield, and fruit increases lignin concentration, reducing the severity of rust on quality of strawberry (Fragaria x ananassa Duch.). The doses of 2 seedlings in nutrient solution (Pé rez et al., 2020). In addition, in kg B ha-1 and 3 kg Zn ha-1 lead to the highest number and yield of wheat (T. aestivum L.) seedlings, B and Mn applications have fruits, increase soluble solids and ascorbic acid contents, and B and significant effects on the reduction of the number of lesions per Zn absorption. These results indicate that the interaction of B x Zn leaf between booting and milk stages (Simoglou and Dordas, 2006). increase the quantity and quality of strawberry fruit. On the other Furthermore, the combined application of B, Mn and Zn increases Frontiers in Plant Science 07 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 in plant growth, shelling ratio and chlorophyll concentration in pea Boron and aluminum in plants plants due to synergism between the elements (El-Aidy et al., 2021). In another case, antagonistic effects were reported; for example, in Aluminum (Al) is also a non-functional element in plants. The tobacco leaves, the increase of B concentrations diminishes the Mn/ interaction between B and Al has been proposed to be beneficial, with Fe ratio, due to a rise in the Fe concentration and a fall in Mn levels B promoting the efflux of H+ thus regulating H+-ATPase activity in (Ali et al., 2015). the plasma membrane, and reducing the demethylation of pectin to weaken Al binding to carboxyl groups; nevertheless, the processes and mechanism involved in alleviating Al toxicity are still not clear Boron interaction with iron (Li et al., 2017; Li et al., 2018; Yan et al., 2021). Aluminum binds to the cell wall and induces changes in the content, proportion, and It has been suggested that B promotes the absorption and structure of cell wall components, particularly in pectin and longdistance transport of Fe in plants (Alvarez-Tinaut, 1980). In hemicellulose fractions (Zhou et al., 2015; Xu et al., 2022; Yan tomato growing hydroponically, B levels influence Fe absorption and et al., 2022). Furthermore, Al has been found to alter the translocation paralleling the dry matter production. Fe absorption extensibility, rigidity, and porosity of the cell wall (Illé s et al., 2006; varied with B supply in the same way and in a similar pattern to Zhou et al., 2015; Yan et al., 2022). In Poncirus trifoliata (trifoliate growth under the same B levels (Alvarez-Tinaut, 1980). This points to orange), it was reported that B application decreases the levels of an indirect influence of B on Fe absorption, through increasing growth hydrogen peroxide (H2O2), malondialdehyde (MDA), and lignin and hence Fe (and other nutrients too) demands. Another interaction contents in roots of Al-treated plants (Yan et al., 2022). These between B and Fe has been reported in the reallocation of apoplastic Fe results suggest that B could be involved in a mechanism that in root, an essential Fe storage pool in plants. It is known that B can prevents the inhibitory effects of Al on root growth. affect the dimerization of pectin rhamnogalacturonan-II (O’Neill et al., Among the various components of the cell wall, lignin is 2004). Peng et al. (2021) reported that a decreased the abundance of the important as it is associated with mechanical properties and is a rhamnogalacturonan-II dimer compromised the reallocation of Fe vital indicator used to assess Al tolerance in plants (Wang and Kao, from roots to shoots and severely impaired root growth. This 2006; Smith et al., 2011). In tree species, it was observed that B- information suggest that B can regulate the chelation of Fe by the deficiency induces the upregulation of lignin monomer cell wall, by its role in the cell wall biosynthesis and thus apoplastic biosynthesis, via the modification in the expression of several Fe reallocation. transcription factors, including MYBs, WRKYs and NACs in Norway spruce (Picea abies L.). On the other hand, in poplar (Populus tremula L.), PtrMYBs are upregulated under B- Beneficial elements and deficiency, transcription factors that are orthologues of AtMYB58 toxic elements and AtMYB63, which are regulators of lignin synthesis (Su et al., 2019). Additionally, plants under B-starvation display changes in Boron interaction with silicon the phenylalanine metabolic pathway, which promotes lignin accumulation, suggesting that B is related to lignin content and Silicon (Si) is a beneficial element for plants, which has been its metabolic pathway in the cell wall (Wu et al., 2017). It could also demonstrated by several studies in many species and environmental be suggested that the effect of B in alleviating Al toxicity is mainly conditions (Rizwan et al., 2015; Debona et al., 2017; Etesami and due to the formation of RGII-B complexes, which help to stabilize Jeong, 2018; Pavlovic et al., 2021; Song et al., 2021). In barley the cell wall (Li et al., 2017). In this regard, B increases the content (Hordeum vulgare L.), Akcay and Erkan (2016) described that the of RG-II (KDO, 2-keto-3-deoxyoctonic acid) to create more borate- combined application of B and Si increased the transcription levels RGII complexes, and in turn reduces the methyl esterification of of BOR2 transporter efflux gene, involved in the B detoxification in pectin, thus forming more negative charges to immobilize Al3+ in the apoplast. Interestingly, the same authors described higher cell wall pectin. In fact, Al binds to the negatively-charged carboxyl expression levels in the shoot in comparison to the root which groups of pectins, and both Al-induced ROS and free Al3+ can could explain the preventive role of the B accumulation and the disrupt the cell wall, producing modifications that could in turn increased tolerance to high B (Miwa and Fujiwara, 2010). reduce elasticity, due to the cleavage of polysaccharides or methyl Accordingly, Akcay and Erkan (2016) showed that exist a certain esterification (Yang et al., 2010; Ranjan et al., 2021). However, when degree of competence in the B transport system that favors Si B is applied, it binds to pectin hence reducing the entry of Al to the uptake, being also the mechanism proposed in oilseed rape grown cell and minimizing the toxic effects of Al (Riaz et al., 2019). In under B excess (Liang and Shen, 1994). In fact, B can be transported many plant species, the plasma membrane H+-ATPase has been through the multifunctional HvNIP2;1 transporter in barley and studied and Al toxicity can affect both its expression and post- rice plants (Schnurbusch et al., 2010; Mitani-Ueno et al., 2011) translational activity (Zhang et al., 2017). In this regard, the work of (Table 2). HvNIP2;1 transporter is the homolog of OsLsi , an influx Yan et al. (2021) shows that B could alleviate the Al-induced Si transporter, suggesting that both elements use the same inhibition in the activity of the H+-ATPase by promoting the transporter system in plants. In addition, a genome-wide activity of the H + -ATPase and thus H + efflux, therefore association mapping supports the idea that HvLsi6 is required for weakening the acidic intracellular environment produced by Al. efficient B transport in barley (Jia et al., 2021). In this case, B also lowers the synthesis of pectin and the activity of Frontiers in Plant Science 08 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 pectin methylesterase. This latter point is important to highlight as species. Indeed, important questions regarding B x Al, such as the degree of methylation of pectin helps determine the amount of deacidification, signaling pathways and the global up- and down- carboxyl groups that can bind to Al3+ and its sensitivity in different regulation of genes through transcriptomics need to be plant species (Horst et al., 2010). It has also been proposed that B further investigated. promotes alkalization of the root surface of peas. This is regulated by Polar Auxin Transport (PAT), leading to the downstream regulation of the H+-ATPase, consequently alleviating any toxic Boron and cadmium in plants effect produced by Al (Li et al., 2018). Additional effects of B on plants in response to Al stress have been Cadmium (Cd) is a highly toxic heavy metal for plants (Al- described. Working with seedlings of trifoliate orange, Riaz et al. (2018) Khayri et al., 2023). At toxic levels, Cd alters the growth, report changes at a physiological and molecular level, observing development, yield and quality of plants. The symptoms of Cd differences in root length and improved antioxidant activity based on toxicity are easily identifiable as chlorosis that occurs due to blocked the alleviation that B produces in interaction with Al. As described in Fe and Zn uptake, and stunted growth. Cadmium toxicity leads to a this work, this improvement is thought to be produced because the greater production of ROS and to a decrease in the chlorophyll supply of B reduces the uptake of Al in roots and leaves in response to content and photosynthetic activity (Nazar et al., 2012; Haider et al., oxidative damage. According to Yan et al. (2019), in the same species, B 2021). Regarding the B x Cd interaction, the effect has been reported can also reduce Al-driven ascorbate synthesis, by downregulating the to occur in the structural and functional integrity of the cell wall and metabolites involved in the L-galactose pathway. This is believed to be membranes (Nishizono et al., 1987; Riaz et al. 2020). Studies done achieved as B eases the effects of Al by decreasing the redox status and with B have pointed out that the presence of B in fertilizers could activities in the ascorbate-glutathione cycle, via its enzymes ascorbate actually mitigate the toxic effects of Cd on crops by enhancing Cd peroxidase, dehydroascorbate reductase, glutathione reductase, and chelation onto plant cell walls (Qin et al., 2020; Wu et al., 2020b; glutathione peroxidase. Long and Peng, 2023). According to Chen et al. (2019), B affected The molecular mechanisms that underlie the B-induced favorably the antioxidant machinery in rice, increasing the activities alleviation of Al-toxicity in plants are poorly understood. Studies of superoxide dismutase, peroxidase and catalase, mitigating the investigating the gene expression patterns in Sour pummelo (Citrus detrimental effects of Cd-stress. Most of the studies of the B x Cd grandis) roots that respond to B x Al interactions show that B interaction have focused on rice and oilseed rape, such that appears to alleviate Al toxicity by improving the overall ability to diversifying our studies would give more insights about the remove ROS and aldehydes, increasing expression levels of lipid- mitigating effects that B has on Cd in more diverse species. related genes and upregulating cellular transport-related gene Several authors have reported that B can mitigate Cd toxicity in expression (Zhou et al., 2015). Another study of the B x Al plants given that B affects cell wall structures and some components interaction performed in C. grandis supports the alleviation of B- that allow blocking the entry of Cd into the cytosol (Wu et al., induced Al toxicity by finding that it could be attributed to cell wall 2020a; Wu et al., 2020b; Riaz et al., 2021). Several studies showed remodeling by reducing lignin synthesis (via the sugar ATP Binding that B could significantly reduce the Cd accumulation in roots rice Cassette (ABC) transporter ATPase) and increasing the through the downregulating of Nramp1, Nramp5, HMA2, and modification of cell wall. Greater abundance of stress response HMA4 expression of Cd-induced transporters, promoting the proteins, greater cellular regulation and signal transduction adsorption of Cd in cell wall of roots, and activating the (calreticulin-1) confer a possible mechanism for the alleviation of antioxidant enzyme system (Chen et al., 2019; Riaz et al., 2020; Al toxicity induced by B (Yang et al., 2018). More recent studies Riaz et al., 2021). The repressed expression of these Cd transporter report that B increases the expression of genes (OsSTAR1 and genes by both B and Cd are linked to the reduction of Cd uptake OsSTAR2) that are responsible for reducing the Al content in cell and transportation, diminished Cd accumulation in both walls in rice (Table 2). Furthermore, it significantly increases the aboveground and belowground level in rice plants (Huang et al., expression of OsALS1, thus facilitating the transfer of Al from the 2021). It is thought that B decreases the expression of some Cd- cytoplasm to the vacuole (Zhu et al., 2019). A transcriptomic study induced transporter genes such as HMA2, NRAMP1 and some ABC also reports that B could lessen Al toxicity by inducing the genes; hence, relieving Cd toxicity and its accumulation in rice expression of several genes, including PtALMT4 and PtALMT9, seedlings by restraining its uptake and translocation from root to PtALS1 and PtALS3, and PtSTAR1, which is responsible for shoot, improves the tolerance and chelation ability that rice can reducing Al deposition of the cell wall in trifoliate orange plants have toward Cd (Table 2). In wheat, the expression of Cd genes subjected to Al toxicity (Yan et al., 2022). Based on these reports, B (TCONS1113, TRIAE1060, TRIAE5370 and TRIAE5770) in the could actually be responsible for regulating several genes and presence of B was also boosted (Qin et al., 2022), proposed that pathways sensitive to Al, reducing the distribution of Al in the the application of B could inhibit significantly Cd uptake and subcellular components after its addition. translocation through the regulation of Cd transporter genes Therefore, there are several interesting aspects of plant response either at the seedling or elongation phase. mechanisms to Al toxicity; nevertheless, more research is needed to The molecular interactions that B exerts with different elements identify molecular players associated with B and Al in different still need to be elucidated, particularly as these interactions may Frontiers in Plant Science 09 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 FIGURE 1 Molecular interaction of B with other elements. (1). Boron interaction with Ca2+. Boron deficiency has been associated with changes in the expression of Ca2+ genes (ACA, CAX, CNCG) that are activated to restore Ca2+ homeostasis within the cytosol. (2) Boron interaction with N. Under B deficiency, nitrate transporters are downregulated affecting H+-ATPase transcripts and leading to ammonium accumulation along with elevated glutamine and asparagine production. (3) Boron interaction with K. AGP transcripts have been studied in the B x K relationship. Under B deficiency, these proteins are downregulated leading to changes in the membrane-cytoskeleton continuum in which an unknown cascade of signals is thought to be activated. (4) Boron interaction with Al. B has been studied as an alleviator of Al toxicity. Through different mechanisms and regulation of transport-related genes, B induces protein expression to reduce the deposition of Al in the cell wall and diminish its toxicity by importing it into vacuoles. (5) Boron interaction with Si. Si and B interact using the same NIP transporters, possibly allowing for B detoxification when found in high levels. (6) Boron interaction with Cd. Interestingly, B and Si when combined display an inhibitory activity over Cd transporters, accounting for the elimination of Cd toxicity. (7) Boron interaction with P. Under low B conditions, changes in BnaPT transporter expression regulates P content. Otherwise, under B toxicity and low P conditions, the transporters BnaC3 and SPX3 are upregulated to balance P content. (8) Boron interaction with Zn. Zinc finger proteins are upregulated in response to B toxicity. It is believed that these proteins regulate B content by stress signal transduction pathways to improve plant growth and development. These observations have been studied in different plant species and are not necessarily equivalent in all species. Created with Biorender. vary between species. Figure 1 shows a general scheme of the with B which can be direct or indirect with other plant nutrients. molecular interactions of B with other elements, in both deficient Furthermore, the interactions of B with other plant nutrients are and excess conditions. highly complex and their effects can be antagonistic or synergistic, depending on plant species/varieties and the environment. Environmental factors may provoke B deficiency even in the Conclusions and future perspectives presence of higher quantities of B in the soil. Moreover, B addition through fertilization in some cases, could enhance crop productivity Boron can be present at insufficient or excessive levels in the soil. by alleviating metabolic alterations displayed by toxic levels of Al and The means by which plants cope with such differences requires a heavy metals like Cd, reducing overall yield losses. Since application study of intra- and inter-species genetic variability, together with new of B in fertilizers is highly cost-effective, its use in fertilization discoveries about the mechanisms of tolerance to B toxicity, that programs should be properly evaluated alongside a determination could facilitate the breeding of new varieties with satisfactory yields in that could define whether application of B is more beneficial when soils with high levels of B. Nevertheless, several lines of evidence added to the soil or to the leaves. In all, B plays important roles in the indicate that extreme deficient or toxic levels of B may be responsible nutrient interactions within plants; however, important basic for secondary effects related with impaired plant growth, insufficient questions related with B being directly or indirectly involved when nutrient uptake and altered nutrient homeostasis due to interactions interacting with certain nutrients deserve further research efforts. Frontiers in Plant Science 10 frontiersin.org Vera-Maldonado et al. 10.3389/fpls.2024.1332459 Author contributions Conflict of interest PV-M: Writing – original draft. FA: Writing – review & editing. The authors declare that the research was conducted in the MR-D: Writing – review & editing. PC-F: Formal Analysis, Writing absence of any commercial or financial relationships that could be – review & editing. BS-C: Writing – review & editing. AN-N: construed as a potential conflict of interest. Writing – review & editing. CI-B: Conceptualization, Funding The author(s) declared that they were an editorial board acquisition, Project administration, Resources, Supervision, member of Frontiers, at the time of submission. This had no Writing – original draft, Writing – review & editing. impact on the peer review process and the final decision. Funding Publisher’s note The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The authors All claims expressed in this article are solely those of the authors declare financial support was received for the research, authorship, and do not necessarily represent those of their affiliated organizations, and/or publication of this article through ANID FONDECYT Regular or those of the publisher, the editors and the reviewers. Any 1201749 (CI-B), ANID/FONDAP/15130015, ANID FONDECYT product that may be evaluated in this article, or claim that may Regular 1211856 (MR-D), ANID FONDECYT Postdoctoral 3220674 be made by its manufacturer, is not guaranteed or endorsed by (PC-F), and ANID Doctoral scholarship 21211268 (PV-M). the publisher. References Agbenin, J., Lombin, G., and Owonubi, J. (1991). Direct and interactive effect of Beato, V., Rexach, J., Navarro-Gochicoa, T., Camacho-Cristó bal, J., Herrera- boron and nitrogen on selected agronomic parameters and nutrient uptake by cowpea Rodrı́guez, B., Maldonado, J., et al. (2010). 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