Micronutrient Deficiency and Toxicity in Plants: Comparison
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Please note this is a comparison between Version 2 by Rita Xu and Version 1 by Sowmya Poosapati.

Micronutrients are essential for plants. Their growth, productivity and reproduction are directly influenced by the supply of micronutrients. Currently, there are eight trace elements considered to be essential for higher plants: Fe, Zn, Mn, Cu, Ni, B, Mo, and Cl. Possibly, other essential elements could be discovered because of recent advances in nutrient solution culture techniques and in the commercial availability of highly sensitive analytical instrumentation for elemental analysis.

  • micronutrients
  • proteomics
  • genomics
  • nutrient toxicity

1. Introduction

Essential nutrients (macro and micro) are required by plants for appropriate functioning and development. The significance of micronutrients in plant nutrition is well recognized. Micronutrients comprise less than 1% of the dry weight of most plants and are vital for their growth [1]. Plant classified micronutrients include boron, chlorine, copper, iron, manganese, molybdenum, nickel and zinc, which are vital for completion of the plant’s life cycle (Figure 1) [2]. They are also essential to maintain the stability of proteins and cellular structures. Through their interactions with other physiologically active molecules and enzymes, micronutrients play an essential role in the biosynthesis of proteins, nucleic acids, cofactors, carbohydrate metabolism, lipid metabolism, stress tolerance, chlorophyll maintenance, electron transport, anti-oxidative systems and much more. Hence access to micronutrients is critical for optimum crop nutrition and development (Figure 2) [3]. The bioavailability of micronutrients is heavily influenced by climatic factors like drought, severe rain, waterlogging or salinity [4]. Energy metabolism, primary and secondary metabolism, cell defense, gene expressions and regulations, hormone sensing, signal transduction, and reproduction are all influenced by micronutrients. The proportion of micronutrients in soil is determined by the geological substrate and pedogenesis management strategies. The ideal concentration of each micronutrient in the crop is influenced by chemical and physical features of the soil, such as soil pH, nutrient availability, clay minerals, microbial activity, amount of organic matter in the soil, quantity of other nutrients, and other factors that might affect micronutrient absorption and efficacy (Table 1). Although the fraction of micronutrients available in the soil may exceed a single plant’s requirements, the accessible proportion may be insufficient for all, resulting in nutritional deficiency in the crop. In Indian soils, improper nutrient management leads to multi-nutrient deficits [5]. Growth of the plant is constrained either by lack of micronutrients, nutrient toxicity or soil conditions.
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Figure 1. Versatile role of micronutrients in plant’s growth and development.
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Figure 2. Micronutrients involved in the growth and development of different parts of the plant.
Table 1. Micronutrients, their modes of intake and their concentrations in the leaves.
S. No. Micronutrient Year of Discovery Ionic Form of Intake Normal Value (ppm) Deficient Value (ppm) Toxic Value (ppm)
1 Boron (B) Warington (1937)
Table 2. Summary of micronutrient functions and deficiency symptoms.
S.No. Micronutrients Representative Constituents/Proteins Functions Symptoms of Deficiency Probable Cause of Deficiency & Method of Correction References
H2BO3, H
1 Zinc (Zn) Cu–Zn superoxide, Peptide deformylase, enzyme carbonic anhydrase (CA), α-Mannosidase, Matrix metalloproteinase

alcoholic dehydrogenase, and superoxide dismutase (SOD)		2BO3−, HBO32−, BO33− 10–20 5–10 50–200
role in nitrogen metabolism and photosynthesis, controls the concentration of auxin in plants, increases seed viability and seedling vigor, protection against abiotic and biotic stresses Reduced vigor, chlorotic leaves, white streaks parallel to leaf blade, slow growth, restricted RNA and protein synthesis Low Zn in soil, high soil pH—lower soil pH, apply foliar spray or add Zn to soil. [8,[9,810,11,][9][10][12,1113,14,]15,16][12][13][14][15][16] 2 Chlorine (Cl) Broyer et al. (1954) Cl− 100–500 Less than 100 500–1000
2 Copper (Cu) Plastocyanin Cu-Znsuperoxide, Ascorbate, Cu-metallothionein, biosynthesis oxidase, Mo-cofactor, dismutase, polyphenol or catechol oxidase, tyrosinase, laccase, Cytochrome-C oxidase, Ethylene receptor ascorbic oxidase and Polyphenol oxidase saves plants from diseases, improves the fertility of male flower, concerned with the oxidation of iron in plants Leaf tips dries, break down and dies, ragged leaves, reduced growth Low soil Cu, high organic matter—apply foliar spray or add Cu to soil [17,18,19,20,,26][21,17][22,1823,24,][19][20][21][22][23][24]25[25][26] 3 Copper (Cu) Lipman and Mackinney (Sachs 1931) Cu2+ 5–30 2–5 100–200
3 Iron (Fe) Aconitase, dismutase, Xanthine dehydrogenase, Ferredoxin, porphyrin NADH, Succinate, Leg hemoglobin, heme and heme enzymes peroxidase oxidase,

dehydrogenase, Nitrate reductase oxidoreductases, Thioredoxin reductase, Cytochrome P450, Aldehyde oxidase, Catalase, Nitrite reductase, Lipoxygenase, Alternative oxidase, Fe-superoxide Ferritin and other functional metallic proteins		 Present in haemoglobin of the leguminous root nodules, leg-haemoglobin and is involved in nitrogen fixation as a constituent of ferredoxin Interveinal, creamy chlorosis on apical leaves, stunted shoots, reduced yield Waterlogged soil, over fertilized, excess of elements like Mn—spraying plant with iron rich fertilizer, chelated iron powder or blood meal directly to the soil [27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46][27][28][29][30][31][32][33][34][35][36][37][38][39][40]
stunted/restricted growth, stubby roots, interveinal chlorosis, non-succulent tissue, wilting
Low soil Cl especially in soils subjected to leaching—apply Cl containing fertilizer [55,59][55][59]
Micronutrient toxicity also leads to various phenotypic, as well as genotypic, changes in the plants (Table 3). When the internal quantity of the micronutrients surpasses the threshold, they cause phytotoxicity. To deal with the scenario, a plant develops a set of tactics at both the proteomic and genetic levels (Table 4 and Table 5). Plants with tolerance to heavy metals have also been examined for proteomic alterations, revealing one more field of molecular application and its regulation [60]. Some plants respond to nutrient toxicity by increasing nutrient efflux and activating detoxifying pathways, whereas others can tolerate high concentrations of certain micronutrients because they have developed systems to store these and utilize them for defensive functions (Figure 4).
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Figure 4. An outline presenting the molecular and the biochemical mechanisms involved in micronutrient cytotoxicity in plants.
Table 3. Micronutrient toxicity.
S. No. Micronutrients Type
Table 5. Examples of genomic responses of plants to nutritional stress.
Metals Plant SpeciesSymptoms of Excess Usage References
Tissue Method of Identification Gene Functions Regulation References
1 Zinc (Zn) Metal Inhibited root growth, young leaf chlorosis, interveinal mild chlorosis in young leaves starting from base and spread towards apex followed by reddish brown coloration, rolling of leaves [
Boron (B) Arabidopsis thaliana61]
Root qRT-PCR SHB1/HY1 B-tolerance Up [72] 2 Copper (Cu) Metal Reduced vigor, inhibited root growth/root damage, older leaves develop orange or pink coloration followed by severe rolling of leaf margins due to loss in turgidity
[41][42][
343][44][45 Iron (Fe)][46] Metal Reduced yield, bronzing and stippling of leaves, and, in some plants, acid is secreted from the roots 4 Iron (Fe) Sachs (1860) Fe2+, Fe3+ 100–500
4 Manganese (Mn) MetalLess than 50 More than 500
4 Tissue injury, leaf sheath and lower parts of stem in cereal normally consist of minute brown spots, legumes develop brown or purple spots over leaf margin, deficiency symptoms of other nutrients
5 Boron (B) Metalloid Toxicity results in dark brown speckles or necrosis on the edge of older leaves, cupped and wrinkled young leaves
6 Molybdenum (Mo) Metal Leaf malformation, tints of golden yellow or blue color in leaves
7 Chlorine (Cl) Non metal Death of leaf margin, leaves are reduced in size and number, have bronze or yellow coloration with brown or scorched leaf margins.
Table 4. Proteomic response of plant to micronutrient stress.
Metal Plant Species Plant Part Extraction Method Protein Name Function Regulation References
Boron (B) Citrus grandis Root iTRAQ Alcohol dehydrogenase 1 Energy metabolism Down [62]
Serine/arginine- rich 22 Nucleic acid metabolic process Down
Clathrin light chain protein Cellular cytoskeleton and transport Up
Manganese (Mn) Malic enzyme, Mn-superoxide, amidohydrolase, primary component of water-splitting enzyme related to photosystem II, PEP carboxylase, Allantoate, Iso-citrate lyase, dismutase PEP-carboxykinase Involved in tricarboxylic acid cycle in oxidation and reduction reactions, activates several enzymes such as oxidoreductases, hydrolases and lyase, also autocatalyzes isocitrate dehydrogenase, malic dehydrogenase, glycocyaminase and D-alanyl synthase. Reduced quality and yield, stunted plants, intervenial chlorosis in leaves, yellow cast in deficient areas. Death of basal leaves, decreased cold hardiness, growth of lateral roots stopped, inhibition of nitrate metabolism. Low soil Mn, high soil pH due to over liming—lower soil pH, apply foliar spray or add Mn to soil [47,4748,][4849,][4950,]51,52][[50][51][52]
Peroxiredoxin IIF 5
Cellular response to stress Down 5Manganese (Mn) Mchargue (1922) Mn2+ 20–300 15–20 300–500
Boron (B) Rhamnogalacturonan II increases cell wall thickness and flower production, as well as retention, pollen tube elongation and germination, along with seed and fruit development. It also helps in the translocation of photosynthates. It inhibits IAA oxidation and gives drought tolerance to crops Thick and leathery old leaves, shoot tip death, rosette leaves with short internodes, excess branching, short, twisted and/or ruptured petioles, vegetables with hollow heart, small and deformed/no fruits with cork spots chlorosis, stubby roots, inhibited nitrogen metabolism. Low soil B especially on sandy soils or light textured soils—apply foliar spray or add B to soil [53,54,55,56][53][54][55][56
Phospholipase C2] Signal transduction Down 6 Molybdenum (Mo) Arnon and Stout (1939) MoO42− 0.1–2.0 0.03–0.15
6More than 100
Molybdenum (Mo) nitrogenase, sulphite oxidase, nitrate reductase Aldehyde oxidase and xanthine oxidase/dehydrogenase aids in the synthesis of ascorbic acid, formation of pollens and anthers, acts as a remedy to excessive copper, manganese and zinc stunted growth with twisted stems, leaves turning pale green, necrotic area in leaves along the mid rib between veins and along leaf edges
Arabidopsis thalianaLow soil pH, low Mo content in soil—inoculate seed with Mo, apply foliar spray or add Mo to soil Leaf[ 2-DE, LC-MS/MS Rubisco activase Photosynthesis Up [ 7 Zinc (Zn) Sommer and Lipman (1926) Zn2+ 27–150 10–20 100–400
Micronutrient depletion develops in the soil as a result of farming techniques, such as intensive farming, monocultures, and acid soil liming, which affect the plants in various ways (Table 2, Figure 3). When nutrient demand exceeds the rate of supply, the plant frequently switches to alternative metabolic pathways, which are often dependent on limiting micronutrients. A decrease in one micronutrient content might reduce the bioavailability of other nutrients in the soil [6]. Although, in certain cases, plants seem unable to detect a deficit because micronutrient availability is impacted by organic matter content, soil pH, adsorptive surfaces, and other biological, chemical, and physical environmental conditions. Prolonged negligence of micronutrient supplementation and aversion of organic fertilizers are major contributors to micronutrient insufficiency and plants respond to these conditions in a variety of ways, by reprogramming transcriptional and translational modifications [2]. Identifying metal-tolerant genes and/or proteins is the first step in deciphering the pathways linked with micronutrient stress tolerance [7].
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Figure 3. Symptoms of micronutrient deficiencies in plants.
33
Oryza sativa Root Microarray, qRT-PCR LOC_Os08g30740 ABC transporter Down [73]
LOC_Os10g30156
,
34
,57,63][34][5758][33]][58]
7 Chlorine (Cl) Oxygen-evolving complex Seismonastic movement activates enzymes that are involved in starch utilization which affects germination and energy transfer. Inmoisture-stress conditions chlorine helps in the movement of water into cells and maintenance of that water. Chlorine also controls the opening and closing of stomata on leaf surfaces
Starch synthase Down
LOC_Os10g30080 Xylosyltransferase Down
Citrus sinensis Leaf Illumina sequencing, qRT-PCR Ciclev10017846m Ubiquitin-protein ligase activity Down [74]
Ciclev 10012377m Transcription factor Up Actin 7 Metabolism Down
Ciclev 10009779 m Blue copper protein Up Fructose-bisphosphate aldolase Energy metabolism Up
Zinc (Zn) Arabidopsis thaliana Whole plant qRT-PCR PDR8 Phytochelatin synthesis Up [75] Glycolate oxidase Photosynthesis Down
ABCCI Metabolism Down Coppe (Cu) Sorghum bicolor Leaf 2-DE, MALDI-TOF MS Thymidine kinase
Iron (Fe)Protein translation and synthesis Down [64]
Citrus sinensis Whole plant qRT-PCR Cs3g19420 Ethylene-responsive transcription factor Up [76] Thaumatin-like protein Stress and defense Up
Cs4g12540 Ethylene synthesis Down Maturase K Growth and development Down
Cs9g02930 Flavone synthase Down Alcohol dehydrogenase Oxidation– reduction process Up
Arabidopsis thaliana Root qRT-PCR FRO2 Iron homeostasis Up [77] Oryza sativa Root 2-DE, MALDI-TOF MS Putative peroxidase
Manganese (Mn) Arabidopsis thalianaAnti-oxidation and detoxification Up [65]
Root qRT-PCR and RNA sequencing AT5G05960 Bifunctional inhibitor Down [78] Putative cold shock protein-1 Transcriptional regulation Up
AT4G39940 Glucosinolate Up Putative elongationfactor EF-2 Protein synthesis Down
AT1G15820 metabolism Photosynthesis Up Glutamine synthetase shoot isozyme Amino acid synthesis Down
Citrus sinensis Leaf cDNA-AFLP and qRT-PCR TDF #065-1 Energy metabolism Up [79] Allium cepa Root 2-DE, MALDI-TOF MS Glutaredoxin Defense Up [66]
TDF #073-1 Cell transport Down Ran-binding protein 1 Protein synthesis Down
TDF #103-2 Stress responses Down Cinnamoyl-Co-A-reductase 1 Cell wall synthesis Down
Copper (Cu) Arabidopsis thaliana Whole plant qRT-PCR OsLAC10 Laccase activity Up [80] Proliferation-associated 2 g4 Cell cycle and DNA replication Up
AtLAC11 Lignin biosynthesis Up Iron (Fe) Arabidopsis thaliana Root Itraq, LC-MS Oxidoreductase Hormone metabolism Up [67]
Oryza sativa Whole plant Western blotting, qRT-PCR WAKL4, WAK- like receptor- like kinase Signaling Up
FRO3, ferric chelate reductase 3 Metal handling Up
SAPX, Stromal ascorbate peroxidase Redox Down
IRT3, Iron regulated transporter3 transport Down
Zea may Root LC-MS/MS Aquaporin PIP2-2 Transport proteins Down [68]
Gibberellin receptor GID1L2 Signaling proteins Down
Aldolase Metabolism Up
Actin-2 Cytoskeleton Down
Callreticulin 2 Protein folding Up
Cucumis sativus Root 2-DE, ESI-LC-MS Phosphoglycerate kinase Glycolysis Up [69]
OsHMA4 Copper accumulation Down Malate dehydrogenase Carbohydrate-related metabolism Up
[ Alanine aminotransferase Nitrogen-related metabolism Up
Xylan 1,4-beta-xylosidase Metabolism of sucrose Down
Manganese (Mn) Citrus grandis Root 2-DE, MALDI-TOF MS, LTQ-ESI-MS/MS Acetohydroxyacid isomeroreductase Protein metabolism Down [70]
Maturase K Nucleic acid metabolism Up
Alcohol dehydrogenase Carbohydrate metabolism Up
Iron- sUperoxide dismutase Stress response Down
Valosin- containing protein Cell transport Down
Zinc (Zn) Lactuca sativa Leaf LC-MS/MS, MALDI-TOF MPBQ/MSBQ transferase Photosynthesis Up [71]
Cytosolic fructose-1,6-bisphosphate Energy metabolism Up
74] Putative cellulose synthase Cell wall metabolism Down
Phenylalanine ammonia-lyase Phenylpropanoids biosynthesis Down
Balancing nutritional stressors leads to a multi-genetic response that causes several changes in proteins and genes, which has a direct impact on nearly all biological activities in a live cell. Proteomic and genomic methods can, thus, be instrumental in identifying molecular responses to nutritional stress [2].

2. Molecular Approaches for Understanding Micronutrient Stress Mechanisms in Plants

Micronutrient insufficiency and toxicity might be detected using both proteomic and genomic investigations [6]. The distribution of micronutrients all throughout the soil profile influences their availability to plants. Plants adapt dynamically to maintain nutrient supply and demand in the appropriate range. Proteomics is a popular molecular method for defining full proteomes at the organelle, cell, or tissue level. It is also helpful for comparing proteins under various adverse environmental conditions [90][81]. Sub-proteome analysis of nutrient deficit plants is also becoming popular, which includes analysis of apoplastic fluids, root plasma membrane, microsomal shoot fractions, phloem saps detergent-resistant membranes, thylakoid membranes and root hairs [91][82]. Proteins are the key molecules involved in several biochemical processes, and, as a result, a thorough understanding of stress induced genomic and proteomic changes aids in deeper understanding of the stress induced pathways. Changes in proteomic expressions are correlated with changes in the gene, transcriptome and metabolism levels. However, alterations at the transcriptional level may not always correspond to changes at the proteomic level. Protein expression is regulated not just at the transcriptional level, but also at the translational and post-translational stages, despite the perception of reciprocity between mRNA and protein [92][83]. As a result, information gathered at the translational and post-translational levels can provide more insight into protein responses, their modifications and functional relationships than genome-based predictions can provide. As proteins act as direct mediators of response, examining these alterations at the proteome level is critical [93][84]. These variations are reflected in the proteome compositions, hence proteomic investigations might be useful in identifying important protein components. These could be used as possible biomarkers in the underlying process. Current proteomic investigations have mostly focused on detecting quantitative changes and have relied on comparative proteomic techniques that include two-dimensional gel electrophoresis (2-DE) followed by mass spectrometry analysis (MS). This should lead to a better knowledge of the interactions between various elements, as well as the plant’s responses to environmental conditions at various phases of growth and development. The genome of a life form is consistent, but the proteome is much more complex because protein expression changes with time and environmental factors [94][85]. Several researchers used transcriptome analysis to examine the expression patterns of genes in plants under heavy stress throughout the last decade. Gene expression at the mRNA level may be used to determine plant responses to a micronutrient buildup (Table 5) [95][86]. Furthermore, transcriptional analysis has some drawbacks, such as a lack of correlation between changes in mRNA expression and changes in their related proteins. By combining this method with genotyping technologies, researchers are able to quickly identify genes and networks that coordinate accumulation of elements in plants. A detailed summary of different genomic and proteomic studies carried out using different micronutrients is listed below.

2.1. Boron

Boron deficiency develops as a result of decreased root respiration, advanced cellular transport, rise in antioxidants and ROS-scavenging proteins [96][87]. Total proteins in boron deficit white lupin (Lupinus albus) root extracts were analyzed using 2D-PAGE, and 128 proteins were determined using mass spectrometry, all of which were involved in cell structure and metabolism, protein metabolism, energy pathways and defense mechanism [97][88]. ITRAQ study of the roots of Citrus sinensis seedlings subjected to Boron deficiency revealed a rise in level of 164 proteins, as well as reduction in level of 225 proteins [96][87]. Many of these proteins were involved in signal transduction, cell transport, stress responses, nucleic acid metabolism, protein metabolism, carbohydrate metabolism, biological regulation, lipid metabolism, cytoskeleton metabolism and energy metabolism. Boron-toxicity-responsive proteins have been identified through MS analysis in research carried out on the leaves of Citrus sinensis and Citrus grandis (B- tolerant citrus species). Toxicity to boron is relatively common in alkaline and saline soils. Boron toxicity increases the amount of PSI type III CAB in barley leaves [98][89]. According to the 2D-PAGE research of boron toxicity-responsive proteome in oranges, it was hypothesized energy metabolism and photosynthesis might have resulted in increased CO2 absorption and, hence, resulted in a better continuation of energy balance [82][90]. Proteins associated to ROS-scavengers were highly accumulated in Boron-toxic C. grandis compared to C. sinensis to overcome oxidative stress, according to the analysis of root samples [99][91]. In a separate study, root systems of these citrus species were tested to study the toxicity of boron. In both species, there were 44 up- and 66 down-regulated genes, with Root Hair Defective 3 expressing in C. sinensis and villin4 being repressed. The discovery of boron-toxic-responsive genes involved in the lipid, nucleic acid and energy metabolisms helped researchers to further understand the mechanisms behind boron-toxicity in citrus species [100][92]. Using the SHB1/HY1 gene and increased levels of BOR4 expression, researchers established the boron homeostasis concept in Arabidopsis root samples [72]. According to the findings, excessive boron absorption in plants promotes excess transcription of the BOR4 gene, an efflux type boron transporter, encouraging the exclusion of excessive boron. In Oryza sativa, the genetic diversity linked with boron tolerance was investigated by looking at genes involved in biochemical binding, transport, transcriptional control, and redox homeostasis [73].

2.2. Chlorine

The majority of soils are not chlorine deficit except for sandy soils or soil covering heavy rainfall areas. Reduced leaf surface area, withering of the plant, and limited, highly branching root systems are some of the most common symptoms associated with chlorine deficiency. Near the leaf’s tip, little patches of pale green chlorotic tissue emerge between the major veins. The old leaves show the first signs of chlorine deficit (Figure 3) [2]. The total chlorine content in the plant is very low. Chlorine accumulation in plants occurs in specific tissues, notably leaves or single cells (for example guard cells), causing toxicity. In plants, chlorine-anion transporters have been found as homologous genes. They include ATP binding cassette (ABC) transporters, chloride intracellular channel (CLIL) and nucleotide sensitive–chloride conductance regulator protein (ICln) [101][93]. As proposed by a few researchers with studies on rice (7 members, OsCLC1-7) and Arabidopsis (7 members, AtClCa-g), members of the vast Chloride Channel (CLC) family were found in several organs [102][94]. They have been reported to encode anion channels/ion transporters that are essential in nitrate homeostasis [103][95]. Proteins from the CLC family of Arabidopsis were found in a variety of membranes, including the chloroplast membranes (AtClCd and AtClCf) (AtClCe), vacuolar membranes (AtClCa) and Golgi vesicles (AtClCd and AtClCf), and guard cells (AtClCc). AtClCa expression patterns in roots are very significant. They function as a 2NO3 K/1HC exchanger, capable of accumulating nitrate in the vacuole using electrophysiological and genetic approaches in combination. The Cation-Cl-Cotransporters (CCC) proteins of A. thaliana (At CCC) catalyzed the coordinate symport of K+, Na+, and Cl− in Xenopusl aevis oocytes [104][96]. Recent advances in the identification of novel transporters of Cl− have been reviewed by Li et. al., 2017 [67].

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