ZINC METALLOENZYMES IN PLANTS JORGE CASTILLO-GONZÁLEZ, DÁMARIS OJEDA-BARRIOS, ADRIANA HERNÁNDEZ-RODRÍGUEZ, ANA CECILIA GONZÁLEZ-FRANCO, LORETO ROBLES-HERNÁNDEZ and GUSTAVO ROGELIO LÓPEZ-OCHOA SUMMARY Zinc is an essential plant micronutrient and soil availability protein synthesis. Plants also require zinc for the synthesis of is of great importance in many crops. In plants, zinc is neither tryptophan, a key amino acid in the synthesis of the auxin in- oxidized nor reduced; instead, the significance of zinc stems doleacetic acid. Therefore, zinc also operates in the control of from its physiochemical properties as a divalent cation. Many plant development through its indirect action on auxins. Zinc enzymes include zinc as a cofactor, like the alcohol dehydro- deficiency affects the catalytic activity of all the above enzymes genase (EC 1.1.1.1), superoxide dismutase (EC 1.15.1.1), carbo- and, thus, the metabolic pathways in which they are involved. nic anhydrase (EC 4.2.1.1) and RNA polymerase (EC 2.7.7.6). In The aim of this paper is to analyze the function of Zn in some these cases, it is indirectly evident that zinc deficiency inhibits of metalloproteins involved in plant metabolism. n contrast to Fe, Mn, Cu Zn can give support and stability to an (Hong et al., 2007). Changes in plant me- and Mo, Zn is a transition enzyme by activating it. Higher plants tabolism induced by Zn deficiency include element that is not subject have a number of enzymes containing effects on carbohydrates, proteins, auxins to valence change and, thus, Zn, including alcohol dehydrogenase, car- and damage to membrane integrity. Many it is present in plants only as Zn (II). bonic anhydrase and RNA polymerase Zn dependent enzymes are involved in The element functions mainly as a diva- (Eide, 2011). However, Zn activates many carbohydrate metabolism, especially in lent cation in metalloenzymes and among other enzymes. Even though the changes leaves (Xing et al., 2016). When Zn defi- these functions is the linkage of these caused by Zn deficiency in the growth ciency occurs, carbonic anhydrase activity enzymes to their corresponding substra- and development of plants are highly decreases markedly (Escudero-Almanza tes. In other cases, Zn forms tetrahydric complex, there are some changes that are et al., 2012). In addition, Zn also activates complexes with N and O and, particular- typical and related to the functions of tryptophan synthetase, enzyme responsible ly, is linked to S in a variety of organic this micronutrient in particular reactions for synthesis of tryptophan in indoleacetic compounds (Samreen et al., 2017). Thus, or in specific steps in metabolic pathways acid (IAA) biosynthesis, which is a hete- KEYWORDS / Alcohol Dehydrogenase / Carbonic Anhydrase / Cofactors / Superoxide Dismutase and Aldolase / Tryptophan Synthetase / Received: 01/27/2017. Modified: 02/26/2018. Accepted: 03/29/2018. Jorge Castillo-González. Master student in Fruit Production, Universidad Autónoma de Chihuahua (UACH), Mexico. Dámaris Ojeda-Barrios (Correspondence author). Fruticultural Engineer, M.Sc. in Soil Science and Doctor in Agricultural Sciences, Universidad Autónoma Agraria Antonio Narro, Mexico. Professor, UACH, Mexico. Address: Facultad de Ciencias Agrotecnológicas, UACH. Escorza Nº 900, Col. Centro. C.P. 31000. Chihuahua, México. e-mail: [email protected] Adriana Hernández-Rodríguez. Fruticultural Engineer, M.Sc. in Fruit Productivity and Doctor in Natural Resources UACH, Mexico. Professor, UACH, Mexico. Ana Cecilia González-Franco. Ph.D. in Microbiology, Molecular Biology and Biochemistry, University of Idaho, USA. Professor, UACH, Mexico. Loreto Robles-Hernández. Fruticultural Engineer and M.Sc. in Fruit Productivity, UACH, Mexico. Ph.D. in Plant Pathology, University of Idaho, USA. Professor, UACH, Mexico. Gustavo Rogelio López-Ochoa. Master in Administration, UACH, Mexico. Professor, UACH, México. 242 0378-1844/14/07/468-08 $ 3.00/0 APRIL 2018 • VOL. 43 Nº 4 roauxine (Escudero-Almanza et al., 2012; some respiratory enzymes, accumulation by plants, because micronutrient avail- Hafeez et al., 2013). As already noted, of quinones, and changes in the levels of ability is usually a function of the form Zn is involved in a number of physiologi- amino acids and proteins have also been of the nutrient in the soil, which deter- cal processes in plants. To properly un- reported in Zn deficiency (Broadley mines its mobility to the roots (Ojeda- derstand these processes, it is necessary et al., 2007). In most crops, the typical Barrios et al., 2014). In alkaline soils to consider the Zn-dependent enzymes foliar concentration of Zn required for (pH 7-8.6) the insoluble ZnCO3 is of plants. The objective of this paper is normal growth lies between 15 and 20 formed. Hence, Zn applications to calcar- to analyze the function of Zn in some mg kg-1 of dry matter (Broadley et al., eous soils are not effective and are thus of metalloproteins involved in plant 2007). This metal is a component of nu- limited to non-calcareous ones (Perea- metabolism. merous enzymes such as anhydrases, oxi- Portillo et al., 2010). Zinc deficiency is dases and peroxidases and it performs a widespread in production systems world- Generalities and Classification of critical role in regulating N metabolism, wide. The best diagnosis of Zn deficien- Metalloproteins cell proliferation, photosynthesis, and cy comes from the observation of defi- auxin synthesis. One of the main func- ciency symptoms, combined with foliar Enzymes that depend on tions of Zn is the expression and regula- and soil analysis. Putative values for Zn metal ions as cofactors are of two sorts: tion of genes, as Zn finger transcription extraction from the soil by removal of enzymes activated by metals and metal- factors have been implicated in the regu- the crop at harvest are used to calculate loenzymes. As the name implies, in en- lation of biological processes such as the values of residual Zn in the soil, both zymes activated by metals, catalysis is flowering, photo morphogenesis and soluble and interchangeable (Broadley triggered by the presence of a mono- or pathogen responses (Hafeez et al., 2013). et al., 2012). From this information, it is divalent metal ion on the outside of the Zinc is absorbed by the possible to calculate the extent to which protein. The metal can activate the sub- plant as a chelate, either via leaves or the system has been impoverished at the strate (for instance, Mg2+ with adenosine roots. In long distance transport in the end of a cropping cycle. If the available triphosphate (ATP)) to fit the enzyme di- xylem, it is linked with organic acids or fraction of Zn is lower than the ex- rectly, or to enter in balance with the en- exists as a free, divalent cation. In floe- traction requirement of the following zyme by potentiating its ionic charge to matic sap it is present in high concentra- crop then, a deficiency will occur during produce a stronger, more favorable union tions, linked to low molecular weight or- the next cycle (Ratto and Miguez, 2006). with the substrate or a better catalytic ganic solutes. It can be complexed with environment (Eide, 2011). phospholipids and sulfhydryl groups, Zinc as Metallic Cofactor Metalloproteins (MT) we- where it protects the lipids and proteins re discovered by Margoshes and Valle of membranes against oxidative damage An enzymatic cofactor (1957), who isolated them from the renal (Broadley et al., 2012). is a non-enzymatic component that pro- cortex of horses and identified them as The low levels of IAA motes the catalytic value of an enzyme. proteins able to combine with cadmium in plants with Zn deficiency are a result This definition emphasizes its function (Cd). At first, it was thought that the of the oxidative degradation of super ox- rather than its structure. Almost a third presence of these proteins was related to ide dismutase enzymes (SOD) and cata- of all enzymes require ionic metals for a detoxification mechanism for Cd accu- lase, thus diminishing their activity their catalytic function; hence, ionic met- mulation in the renal tissues of these ani- (Broadley et al., 2012). The characteristic als represent a substantial proportion of mals. Since then, MT have been reported visual symptoms of Zn deficiency in all cofactors. Most trace nutrient metals in all animal phyla examined, and in cer- plants are short internodes and decreased share as a common characteristic, a close tain fungi, plants and cyanobacteria. The foliar expansion, related to a blockage in involvement with enzymes. Many are ac- MT are a set of combined proteins with IAA metabolism (Kirkby and Römheld, tive site components that link the en- low molecular mass, able to bind with a 2004). Transport of Zn from cortical and zyme to the substrate. In this role, they wide variety of metals at a cellular level. epidermal cells of the root to the xylem accept electrons, stabilize tertiary and The MT are mainly located in the cyto- can occur in a simplified form, with Zn quaternary structures and can even regu- plasm but some research has shown their being pumped to the apoplast of the ste- late the speed of metabolic pathways presence in lysosomes and nuclei. In le. Zinc can also be released extracellu- (Eide, 2011). plants, MT concentrations vary consider- larly to the apoplast of the stele in re- Zinc is an ubiquitous and ably, depending on a range of factors gions where the Casparian strip is com- versatile of all the metallic cofactors, such as the kind of organism, tissue, age, pletely formed. Apoplastic flows are gover- with more than 300 enzymes having a development stage, nutritional state, me- ned by cationic interchange in the cell Zn cofactor. Proteins linked to Zn attach tal exposure and on other unidentified wall, Casparian strips and water flow to deoxyribonucleic acid (DNA).