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Proteomic and genomic responses of plants to nutritional stress

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Abstract

Minerals or trace elements in small amount are essential nutrients for every plant, but when the internal concentration exceeds the threshold, these essential elements do create phytotoxicity. Plant responses to elemental stresses are very common due to different anthropogenic activities; however it is a complex phenomenon with individual characteristics for various species. To cope up with the situation, a plant produces a group of strategies both in proteomic and genomic level to overcome it. Controlling the metal stress is known to activate a multigene response resulting in the changes in various proteins, which directly affects almost all biological processes in a living cell. Therefore, proteomic and genomic approaches can be useful for elucidating the molecular responses under metal stress. For this, it is tried to provide the latest knowledge and techniques used in proteomic and genomic study during nutritional stress and is represented here in review form.

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References

  • Ahsan N, Renaut J, Komatsu S (2009) Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 9:2602–2621

    Article  CAS  PubMed  Google Scholar 

  • Akpjnar BA, Lucas SJ, Budak H (2013) Genomics approaches for crop improvement against abiotic stress. Sci World J 2013:1–9

    Article  Google Scholar 

  • Alvarado MM, Morales SG, Tellez LIT, Contreras JVH, Merino FCG (2017) Aluminum enhances growth and sugar concentration, alters macronutrient status and regulates the expression of NAC transcription factors in rice. Front Plant Sci 8:1–16

    Google Scholar 

  • Anderson S, Bankier AT, Barrell BG, deBruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Younget IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    Article  CAS  PubMed  Google Scholar 

  • Appenroth KJ (2010) What are “heavy metals” in plant sciences? Acta Physiol Plant 32:615–619

    Article  CAS  Google Scholar 

  • Arnon DI, Stout PR (1939) The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiol 14:371–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnon DI, Wessel G (1953) Vanadiumas an essential element for greenplants. Nature 172:1039–1040

    Article  CAS  PubMed  Google Scholar 

  • Balammal G, Reddy PJ (2012) Proteomics & genomics—a review. J Sci 2:91–95

    Google Scholar 

  • Brown PH, Welch RM, Cary EE, Checkai RT (1987) Beneficial effect of nickel on plant growth. J Plant Nutr 10:2125–2135

    Article  CAS  Google Scholar 

  • Broyer TC, Carlton AB, Johnson CM, Stout PR (1954) Chlorine-a micronutrient element for higher plants. Plant Physiol 29:526–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broyer TC, Lee DC, Asher CJ (1966) Selenium nutrition of green plants. Effects of selenite supply on growth and selenium content of alfalfa and subterranean clover. Plant Physiol 41:1425–1428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casassola A, Brammer SP, Chaves MS, Martinelli JA, Grando MF, Denardin ND (2013) Gene expression: a review on methods for the study of defense-related gene differential expression in plants. Am J Plant Sci 4:64–73

    Article  Google Scholar 

  • Celma JR, Tsai YH, Wen TN, Wu YC, Curie C, Schmidt W (2016) Systems-wide analysis of manganese deficiency-induced changes in gene activity of Arabidopsis roots. Sci Rep 6:1–16

    Article  CAS  Google Scholar 

  • Chandna R, Ahmad A (2015) Nitrogen stress-induced alterations in the leaf proteome of two wheat varieties grown at different nitrogen levels. Physiol Mol Boil Plants 21:19–33

    Article  CAS  Google Scholar 

  • Chen M, Mishra S, Heckathorna S, Frantzb JM, Krause C (2014) Proteomic analysis of Arabidopsis thaliana leaves in response to acute boron deficiency and toxicity reveals effects on photosynthesis, carbohydrate metabolism, and protein synthesis. J Plant Physiol 171:235–242

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Song Y, Zhuang K, Li L, Xia Y, Shen Z (2015a) Proteomic analysis of copper-binding proteins in excess copper-stressed roots of two rice (Oryza sativa L.) varieties with different Cu tolerances. PLoS ONE 10:1–19

    Google Scholar 

  • Chen H, Lu C, Jiang H, Peng J (2015b) Global transcriptome analysis reveals distinct aluminum-tolerance pathways in the Al-accumulating species Hydrangea macrophylla and marker identification. PLoS ONE 10:1–19

    Google Scholar 

  • Chen Z, Sun L, Liu P, Liu G, Tian J, Liao H (2015c) Malate synthesis and secretion mediated by a manganese-enhanced malate dehydrogenase confers superior manganese tolerance in stylosanthesguianensis. Plant Physiol 167:176–188

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Yang L, Yan X, Liu Y, Wang R, Fan T, Ren Y, Tang X, Xiao F, Liu Y, Cao S (2016) Zinc-finger transcription factor ZAT6 positively regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis. Plant Physiol 171:707–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chenery EM (1948) Aluminum in the plant world. Part I, General survey in dicotyledons. Kew Bull 2:173–183

    Article  Google Scholar 

  • Ciesla A, Mitula F, Misztal L, Stronska OF, Janicka S, Zielinska MT, Marczak M, Janicki M, Ludwikow A, Sadowski JA (2016) Role for barley calcium-dependent protein kinase CPK2a in the response to drought. Front Plant Sci 7:1–15

    Article  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

  • Curci PL, Cigliano RA, Zuluaga DL, Janni M, Sanseverino W, Sonnante G (2017) Transcriptomic response of durum wheat to nitrogen starvation. Sci Rep 7:1–14

    Article  CAS  Google Scholar 

  • D’Hooghe P, Escamez S, Trouverie J, Avice JC (2013) Sulphur limitation provokes physiological and leaf proteome changes in oilseed rape that lead to perturbation of sulphur, carbon and oxidative metabolisms. BMC Plant Biol 13:1–14

    Article  CAS  Google Scholar 

  • Dai H, Cao F, Chen X, Zhang M, Ahmed IM, Chen ZH, Li C, Zhang G, Wu F (2013) Comparative proteomic analysis of aluminum tolerance in Tibetan wild and cultivated barleys. PLoS ONE 8:1–14

    Google Scholar 

  • Dash PK, Cao Y, Jailani AK, Gupta P, Venglat P, Xiang D, Rai R, Sharma R, Thirunavukkarasu N, Abdin MZ, Yadava DK, Singh NK, Singh J, Selvaraj G, Deyholos M, Kumar PA, Datla R (2014) Genome-wide analysis of drought induced gene expression changes in flax (Linum usitatissimum). GM Crops Food 5:106–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng J, Yu HJ, Li YY, Zhang XM, Liu P, Li Q, Jiang WJ (2016) Leaf volatile compounds and associated gene expression during short-term nitrogen deficient treatments in Cucumis seedlings. Int J Mol Sci 17:1–13

    Google Scholar 

  • Ding C, You J, Liu Z, Rehmani MIA, Wang S, Li G, Wang Q, Ding Y (2010) Proteomic analysis of low nitrogen stress-responsive proteins in roots of rice. Plant Mol Biol Rep 29:618–625

    Article  CAS  Google Scholar 

  • Donnini S, Prinsi B, Negri AS, Vigani G, Espen L, Zocchi G (2010) Proteomic characterization of iron deficiency responses in Cucumis sativus L. roots. BMC Plant Biol 10:1–15

    Article  CAS  Google Scholar 

  • Ebong GA, Offiong OE, Ekpo BO (2014) Speciation, distribution and bioavailability of essential elements in waste impacted soils within Niger delta region of Nigeria. Ann Food Sci Technol 15:162–171

    Google Scholar 

  • Finatto T, deOliveira AC, Chaparro C, daMaia LC, Farias DR, Woyann LG, Mistura CC, Soares-Bresolin AP, Llauro C, Panaud O, Picault N (2015) Abiotic stress and genome dynamics: specific genes and transposable elements response to iron excess in rice. Rice 8:2–18

    Article  Google Scholar 

  • Fleck AT, Nye T, Repenning C, Stahl F, Zahn M, Schenk MK (2011) Silicon enhances suberization and lignification in roots of rice (Oryza sativa). J Exp Bot 62:2001–2011

    Article  CAS  PubMed  Google Scholar 

  • Fu L, Zhu Q, Sun Y, Du W, Pan Z, Peng S (2017) Physiological and transcriptional changes of three citrus rootstock seedlings under iron deficiency. Front Plant Sci 8:1–13

    Google Scholar 

  • Fukao Y, Kobayashi M, Zargar SM, Kurata R, Fukui R, Mori IC, Ogata Y (2016) Quantitative proteomic analysis of the response to zinc, magnesium, and calcium deficiency in specific cell types of Arabidopsis roots. Proteomes 4:1–13

    Article  PubMed Central  Google Scholar 

  • Gao M, Liu Y, Ma X, Shuai Q, Gai J, Li Y (2017) Evaluation of reference genes for normalization of gene expression using quantitative RT-PCR under aluminum, cadmium, and heat stresses in soybean. PLoS ONE 12:1–15

    Google Scholar 

  • Gielen H, Remans T, Vangronsveld J, Cuypers A (2016) Toxicity responses of Cu and Cd: the involvement of miRNAs and the transcription factor SPL7. BMC Plant Biol 16:1–16

    Article  CAS  Google Scholar 

  • Gill T, Dogra V, Kumar S, Ahuja PS, Sreenivasulu Y (2012) Protein dynamics during seed germination under copper stress in Arabidopsis over-expressing Potentilla superoxide dismutase. J Plant Res 125:165–172

    Article  CAS  PubMed  Google Scholar 

  • Goel P, Bhuria M, Kaushal M, Singh AK (2016) Carbon: nitrogen interaction regulates expression of genes involved in N-uptake and assimilation in Brassica juncea L. PLoS ONE 11:1–19

    Google Scholar 

  • Guo W, Chen S, Hussain N, Cong Y, Liang Z, Chen K (2015) Magnesium stress signaling in plant: just a beginning. Plant Signal Behav 10:e992287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo P, Qi YP, Yang LT, Ye X, Huang JH, Chen LS (2016) Long-term boron excess induced alterations of gene profiles in roots of two citrus species differing in boron-tolerance revealed by cDNA-AFLP. Front Plant Sci 7:1–16

    Google Scholar 

  • Gupta DS, McPhee K, Kumar S (2017) Development of molecular markers for iron metabolism related genes in lentil and their expression analysis under excess iron stress. Front Plant Sci 8:1–8

    Google Scholar 

  • Han M, Wong J, Su T, Beatty PH, Good AG (2016) Identification of nitrogen use efficiency genes in barley: searching for QTLs controlling complex physiological traits. Front Plant Sci 7:1–17

    Google Scholar 

  • Harmer PM, Benne EJ (1945) Sodium as a crop nutrient. Soil Sci Soc Am J 60:137–148

    Article  CAS  Google Scholar 

  • Hartenian E, Doench JG (2015) Genetic screens and functional genomics using CRISPR/Cas9 technology. FEBS J 282:1383–1393

    Article  CAS  PubMed  Google Scholar 

  • He L, Lu X, Tian J, Yang Y, Li B, Li J, Guo S (2012) Proteomic analysis of the effects of exogenous calcium on hypoxia-responsive proteins in cucumber roots. Proteome Sci 10:1–15

    Article  CAS  Google Scholar 

  • Hettenhausen C, Sun G, He Y, Zhuang H, Sun T, Qi J, Wu J (2016) Genome-wide identification of calcium-dependent protein kinases in soybean and analyses of their transcriptional responses to insect herbivory and drought stress. Sci Rep 6:1–14

    Article  CAS  Google Scholar 

  • Hopff D, Wienkoopb S, Luthjea S (2013) The plasma membrane proteome of maize roots grown under low and high iron conditions. J Proteomics 91:605–618

    Article  CAS  PubMed  Google Scholar 

  • Hossain Z, Mustafaa G, Sakatac K, Komatsua S (2016) Insights into the proteomic response of soybean towards Al2O3, ZnO and Ag nanoparticles stress. J Hazard Mater 304:291–305

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Rampitsch C, Bykova NV (2015) Advances in plant proteomics toward improvement of crop productivity and stress resistance. Front Plant Sci 6:1–15

    Google Scholar 

  • Hu Z, Lv X, Xia X, Zhou J, Shi K, Yu J, Zhou Y (2016) Genome wide identification and expression analysis of calcium-dependent protein kinase in tomato. Front Plant Sci 7:1–11

    CAS  Google Scholar 

  • Huang A, Sang Y, Sun W, Fu Y, Yang Z (2016a) Transcriptomic analysis of responses to imbalanced carbon: nitrogen availabilities in Rice seedlings. PLoS ONE 11:1–26

    Google Scholar 

  • Huang JH, Qi YP, Wen SX, Guo P, Chen XM, Chen LS (2016b) Illumina microRNA profiles reveal the involvement of miR397a in citrus adaptation to long-term boron toxicity via modulating secondary cell-wall biosynthesis. Sci Rep 6:1–14

    Article  CAS  Google Scholar 

  • Huang XY, Deng F, Yamaji N, Pinson SRM, Kashino MF, Danku J, Douglas A, Guerinot ML, Salt DE, Ma JF (2016c) A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun 7:1–13

    Google Scholar 

  • Ibrahim WIW, Singh VA, Hashim OH, Rahman PSA (2015) Biomarkers for bone tumors: discovery from genomics and proteomics studies and their challenges. Mol Med 21:861–872

    Google Scholar 

  • Ibrokhim YA (2016) Genomics era for plants and crop species—advances made and needed tasks ahead. In: Abdurakhmonov I (ed) Plant genomics, Intech, Europe, pp. 3–25

  • Jiang HX, Yang LT, Qi YP, Lu YB, Huang ZR, Chen LS (2015) Root iTRAQ protein profile analysis of two citrus species differing in aluminum tolerance in response to long-term aluminum- toxicity. BMC Genomics 16:1–17

    Article  CAS  Google Scholar 

  • Jiang H, Zhang J, Han Z, Yang J, Ge C, Wu Q (2017) Revealing new insights into different phosphorus-starving responses between two maize (Zea mays) inbred lines by transcriptomic and proteomic studies. Sci Rep 7:1–9

    Article  Google Scholar 

  • Kayum MA, Kim HT, Nath UK, Park JI, Kho KH, Cho YG, Nou IS (2016) Research on biotic and abiotic stress related genes exploration and prediction in Brassica rapa and B. oleracea: a review. Plant Breed Biotechnol 4:135–144

    Article  Google Scholar 

  • Komatsu S, Hossain Z (2017) Preface-plant proteomic research. Int J Mol Sci 18:1–3

    Article  Google Scholar 

  • Komatsu S, Wang X, Yin X, Nanjo Y, Ohyanagi H, Sakata K (2017) Integration of gel-based and gel-free proteomic data for functional analysis of proteins through Soybean Proteome Database. J Proteomics 163:52–66

    Article  CAS  PubMed  Google Scholar 

  • Kosova K, Vitamvas P, Urban MO, Klima M, Roy A, Prasil IT (2015) Biological networks underlying abiotic stress tolerance in temperate crops-a proteomic perspective. Int J Mol Sci 16:20913–20942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koussounadis A, Langdon SP, Um IH, Harrison DJ, Smith AV (2015) Relationship between differentially expressed mRNA and mRNA-protein correlations in a xenograft model system. Sci Rep 5:1–9

    Article  Google Scholar 

  • Kupper H, Andresen E (2016) Mechanisms of metal toxicity in plants. Metallomics 8:269–285

    Article  PubMed  Google Scholar 

  • Leng X, Jia H, Sun X, Shangguan L, Mu Q, Wang B, Fang J (2015) Comparative transcriptome analysis of grapevine in response to copper stress. Sci Rep 5:1–17

    Google Scholar 

  • Leplat F, Pedas PR, Rasmussen SK, Husted S (2016) Identification of manganese efficiency candidate genes in winter barley (Hordeum vulgare) using genome wide association mapping. BMC Genomics 17:1–15

    Article  CAS  Google Scholar 

  • Li W, Lan P (2017) The understanding of the plant iron deficiency responses in strategy I plants and the role of ethylene in this process by omic approaches. Front Plant Sci 8:1–15

    CAS  Google Scholar 

  • Li LQ, Huang LP, Pan G, Liu L, Wang X, Lu L (2017a) Identifying the genes regulated by AtWRKY6 using comparative transcript and proteomic analysis under phosphorus deficiency. Int J Mol Sci 18:1–20

    Google Scholar 

  • Li Q, Li Y, Wu X, Zhou L, Zhu X, Fang W (2017b) Metal transport protein 8 in Camellia sinensis confers superior manganese tolerance when expressed in Yeast and Arabidopsis thaliana. Sci Rep 7:1–11

    Article  Google Scholar 

  • Li Y, Meng J, Yang S, Guo F, Zhang J, Geng Y, Cui L, Wan S, Li X (2017c) Transcriptome analysis of calcium- and hormone-related gene expressions during different stages of peanut pod development. Front Plant Sci 8:1–15

    CAS  Google Scholar 

  • Liebig BJ (1840) Chemistry in its application to agriculture and physiology. Taylor and Walton, London, pp 92–165

  • Lin YF, Hassan Z, Talukdar S, Schat H, Aarts MGM (2016) Expression of the ZNT1 zinc transporter from the metal hyperaccumulator Noccaea caerulescens confers enhanced zinc and cadmium tolerance and accumulation to Arabidopsis thaliana. PLoS ONE 11:1–30

    Google Scholar 

  • Lipman CB, Mackinney G (1931) Proof of the essential nature of copper for higher green plants. Plant Physiol 6:593–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Wu H, Ji C, Wei L, Zhao L, Yu J (2013) An integrated proteomic and metabolomic study on the chronic effects of mercury in Suaeda salsa under an environmentally relevant salinity. PLoS ONE 8:1–13

    Google Scholar 

  • Liu T, Chen JA, Wang W, Simon M, Wu F, Hu W, Chen JB, Zheng H (2014) A combined proteomic and transcriptomic analysis on sulfur metabolism pathways of Arabidopsis thaliana under simulated acid rain. PLoS ONE 9:1–11

    Google Scholar 

  • Liu C, Cheng YJ, Wang JW, Weigel D (2017a) Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat Plants 3:742–748

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Luo L, Wang X, Shen Z, Zheng L (2017b) Comprehensive analysis of Rice lacase gene (OsLAC) family and ectopic expression of OsLAC10 enhances tolerance to copper stress in Arabidopsis. Int J Mol Sci 18:1–16

    Google Scholar 

  • Liu W, Xiong C, Yan L, Zhang Z, Ma L, Wang Y, Liu Y, Liu Z (2017c) Transcriptome analyses reveal candidate genes potentially involved in Al stress response in Alfalfa. Front Plant Sci 8:1–11

    Google Scholar 

  • Liu X, Lin Y, Liu D, Wang C, Zhao Z, Cui X, Liu Y, Yang Y (2017d) MAPK-mediated auxin signal transduction pathways regulate the malic acid secretion under aluminum stress in wheat (Triticumae stivum L.). Sci Rep 7:1–12

    Article  Google Scholar 

  • Liu Y, Meng Q, Duan X, Zhang Z, Li D (2017e) Effects of PEG-induced drought stress on regulation of indole alkaloid biosynthesis in Catharanthus roseus. J Plant Interact 12:87–91

    Article  Google Scholar 

  • Lucini L, Bernardo L (2015) Comparison of proteome response to saline and zinc stress in lettuce. Front Plant Sci 6:1–12

    Article  Google Scholar 

  • Lv Q, Wang L, Wang JZ, Li P, Chen YL, Du J, He YK, Bao F (2017) SHB1/HY1 alleviates excess boron stress by increasing BOR4 expression level and maintaining boron homeostasis in Arabidopsis roots. Front Plant Sci 8:1–13

    Google Scholar 

  • Ma CL, Qi YP, Liang WW, Yang LT, Lu YB, Guo P, Ye X, Chen LS (2016) MicroRNA regulatory mechanisms on Citrus sinensis leaves to magnesium-deficiency. Front Plant Sci 7:1–16

    PubMed  PubMed Central  Google Scholar 

  • Marino D, Ariz I, Lasa B, Santamaria E, Fernandez-Irigoyen J, Gonzalez-Murua C, Tejo PMA (2016) Quantitative proteomics reveals the importance of nitrogen source to control glucosinolate metabolism in Arabidopsis thaliana and Brassica oleracea. J Exp Bot 67:3313–3323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marrocco I, Altieri F, Peluso I (2017) Measurement and clinical significance of biomarkers of oxidative stress in humans. Oxid Med Cell Longev 2017:1–32

    Article  Google Scholar 

  • Masood A, Iqbal N, Khan NA (2012) The role of ethylene in alleviation of cadmium induced photosynthetic capacity inhibition by sulfur in mustard. Plant Cell Environ 35:524–533

    Article  CAS  PubMed  Google Scholar 

  • Massel K, Campbell BC, Mace ES, Tai S, Tao Y, Worland BG, Jordan DR, Botella JR, Godwin ID (2016) Whole genome sequencing reveals potential new targets for improving nitrogen uptake and utilization in Sorghum bicolor. Front Plant Sci 7:1–15

    Article  Google Scholar 

  • Mchargue JS (1922) The role of manganese in plants. J Am Chem Soc 44:1592–1598

    Article  CAS  Google Scholar 

  • Meisrimler CN, Wienkoop S, Lyone D, Geilfus CM, Luthje S (2016) Long-term iron deficiency: tracing changes in the proteome of different pea (Pisum sativum L.) cultivars. J Proteomics 140:13–23

    Article  CAS  PubMed  Google Scholar 

  • Meng F, Luo Q, Wang Q, Zhang X, Qi Z, Xu F, Lei X, Cao Y, Chow WS, Sun G (2016) Physiological and proteomic responses to salt stress in chloroplasts of diploid and tetraploid black locust (Robinia pseudoacacia L.). Sci Rep 6:1–15

    Article  CAS  Google Scholar 

  • Minic Z (2015) Proteomic studies of the effects of different stress conditions on central carbon metabolism in microorganisms. J Proteomics Bioinformatics 8:80–90

    Google Scholar 

  • Monobe MMS, Silva RC (2016) Gene expression: an overview of methods and applications for cancer research. Veterinaria e Zootecnia 23:532–546

    Google Scholar 

  • Mourato MP, Moreira IN, Leitao I, Pinto FR, Sales JR, Martins LL (2015) Effect of heavy metals in plants of the genus Brassica. Int J Mol Sci 16:17975–17998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muneer S, Jeong BR (2015a) Proteomic analysis of salt-stress responsive proteins in roots of tomato (Lycopersicon esculentum L.) plants towards silicon efficiency. Plant Growth Regul 77:133–146

    Article  CAS  Google Scholar 

  • Muneer S, Jeong BR (2015b) Proteomic analysis provides new insights in phosphorus homeostasis subjected to pi (inorganic phosphate) starvation in tomato plants (Solanum lycopersicum L.). PLoS ONE 10:1–18

    Google Scholar 

  • Nadira UA, Ahmed IM, Zeng J, Wu F, Zhang G (2016) Identification of the differentially accumulated proteins associated with low phosphorus tolerance in a Tibetan wild barley accession. J Plant Physiol 198:10–22

    Article  CAS  PubMed  Google Scholar 

  • Nakashita AM, Takahashi AW, Inoue E, Yamaya T, Saito K, Takahashib H (2015) Sulfur-responsive elements in the 39-nontranscribed intergenic region are essential for the induction of sulfate transporter 2; 1 gene expression in Arabidopsis roots under sulfur deficiency. Plant Cell 27:1279–1296

    Article  CAS  Google Scholar 

  • Nazir M, Pandey R, Siddiqi TO, Ibrahim MM, Qureshi MI, Abraham G, Vengavasi K, Ahmad A (2016) Nitrogen-deficiency stress induces protein expression differentially in low-N tolerant and low-N sensitive maize genotypes. Front Plant Sci 7:1–16

    Article  Google Scholar 

  • Neto JBA, Perez MCH, Wimmer MA, Frei M (2017) Genetic factors underlying boron toxicity tolerance in rice: genome-wide association study and transcriptomic analysis. J Exp Bot 68:687–700

    Google Scholar 

  • Nouri MZ, Komatsu S (2013) Subcellular protein overexpression to develop abiotic stress tolerant plants. Front Plant Sci 4:1–7

    Article  Google Scholar 

  • Oh MW, Nanjo Y, Komatsu S (2014) Gel free proteomic analysis of soybean root proteins affected by calcium under flooding stress. Front Plant Sci 5:1–15

    Google Scholar 

  • Okuda A, Takahashi E (1965) The role of silicon. In: Jones IRRJ (ed) The mineral nutrition of rice plant. Hopkins Press, Baltimore, pp 123–146

    Google Scholar 

  • Parvaiz A, Arafat AH, Abdel L, Saiema R, Nudrat AA, Muhammad A, Salih G (2016) Role of proteomics in crop stress tolerance. Front Plant Sci 7:1–14

    Google Scholar 

  • Pavlovic J, Samardzic J, Kostic L, Laursen KH, Natic M, Timotijevic G, Schjoerring JK, Nikolic M (2016) Silicon enhances leaf remobilization of iron in cucumber under limited iron conditions. Ann Bot 118:271–280

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng HY, Qi Y, Lee J, Yang LT, Guo P, Jiang HX, Chen LS (2015) Proteomic analysis of Citrus sinensis roots and leaves in response to long-term magnesium-deficiency. BMC Genomics 16:1–24

    Article  CAS  Google Scholar 

  • Pontigo S, Godoy K, Jimenez H, Moraga AG, Mora ML, Cartes P (2017) Silicon-mediated alleviation of aluminum toxicity by modulation of Al/Si uptake and antioxidant performance in ryegrass plants. Front Plant Sci 8:1–15

    Article  Google Scholar 

  • Qin R, Ning C, Bjorn LO, Li S (2015) Proteomic analysis of Allium cepa var. agrogarum L. roots under copper stress. Plant Soil 401:197–212

    Article  CAS  Google Scholar 

  • Ranty B, Aldon D, Cotelle V, Galaud JP, Thuleau P, Mazars C (2016) Calcium sensors as key hubs in plant responses to biotic and abiotic stresses. Front Plant Sci 7:1–7

    Article  Google Scholar 

  • Reisenauer HM (1960) Cobalt in nitrogen fixation by a legume. Nature 186:375–376

    Article  CAS  Google Scholar 

  • Ren XL, Li LQ, Xu L, Guo YS, Lu LM (2016) Identification of low potassium stress-responsive proteins in tobacco (Nicotiana tabacum) seedling roots using an iTRAQ-based analysis. Genet Mol Res 15:1–13

    Google Scholar 

  • Ribeiro AP, deSouza WR, Martins PK, Vinecky F, Duarte KE, Basso MF, daCunha BADB, Campanha RB, deOliveira PA, Centeno DC, Cançado GMA, deMagalhaes JV, deSousa CAF, Andrade AC, Kobayashi AK, Molinari HBC (2017) Overexpression of BdMATE gene improves aluminum tolerance in Setaria viridis. Front Plant Sci 8:1–12

    Article  Google Scholar 

  • Rios JJ, Ballesta MCM, Ruiz JM, Blasco B, Carvajal M (2017) Silicon-mediated improvement in plant salinity tolerance: the role of Aquaporins. Front Plant Sci 8:1–10

    Article  Google Scholar 

  • Rout JR, Sahoo SL (2013) Antioxidant enzyme gene expression in response to copper stress in Withania somnifera L. Plant Growth Regul 71:95–99

    Article  CAS  Google Scholar 

  • Rout JR, Ram SS, Das R, Chakraborty A, Sudarshan M, Sahoo SL (2013) Copper-stress induced alterations in protein profile and antioxidant enzymes activities in the in vitro grown Withania somnifera L. Physiol Mol Biol Plants 19:353–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy SK, Kwon SJ, Cho SW, Kamal AHM, Kim SW, Sarker K, Oh MW, Lee MS, Chung KY, Xin Z, Woo SH (2016) Leaf proteome characterization in the context of physiological and morphological changes in response to copper stress in sorghum. Biometals 29:495–513

    Article  CAS  PubMed  Google Scholar 

  • Roychoudhury A, Banerjee A (2015) Transcriptome analysis of abiotic stress response in plants. Transcriptomics 3:1–2

    Article  Google Scholar 

  • Sachs J (1860) Vegetationsversuchemit Ausschluss des Bodensüber die Nahrstoffe und sonstigen Ernahrungsbedingungen von Mais, Bohnen, und andereu P flanzen. Landw Versuchs-Stat 2:219–268

    Google Scholar 

  • Sang W, Huang ZR, Qi YP, Yang LT, Guo P, Chen LS (2015) Two-dimensional gel electrophoresis data in support of leaf comparative proteomics of two citrus species differing in boron-tolerance. Data Brief 4:44–46

    Article  PubMed  PubMed Central  Google Scholar 

  • Sang W, Huang ZR, Yang LT, Guo P, Ye X, Chen LS (2017) Effects of high toxic boron concentration on protein profiles in roots of two citrus species differing in boron-tolerance revealed by a 2-DE based MS approach. Front Plant Sci 8:1–19

    Google Scholar 

  • Sangireddy S, Okekeogbu I, Ye Z, Zhou S, Howe KJ, Fish T, Thannhauser TW (2017) Effects of Al3+ and La3+ trivalent metal ions on tomato fruit proteomes. Proteomes 5:1–14

    Article  Google Scholar 

  • Sarasketa A, Gonzalez-Moro MB, Gonzalez-Murua C, Marino D (2016) Nitrogen source and external medium pH interaction differentially affects root and shoot metabolism in Arabidopsis. Front Plant Sci 7:1–12

    Article  Google Scholar 

  • Satbhai SB, Setzer C, Freynschlag F, Slovak R, Kerdaffrec E, Busch W (2017) Natural allelic variation of FRO2 modulates Arabidopsis root growth under iron deficiency. Nat Commun 8:1–10

    Article  CAS  Google Scholar 

  • Sett R (2017) Tolerance of plant in response to abiotic stress factor. Recent Adv Petrochem Sci 1:555–573

    Google Scholar 

  • Shen C, Wang J, Shi X, Kang Y, Xie C, Peng L, Dong C, Shen Q, Xu Y (2017) Transcriptome analysis of differentially expressed genes induced by low and high potassium levels provides insight into fruit sugar metabolism of pea. Front Plant Sci 8:1–16

    Article  Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics and ionomics. Front Plant Sci 6:1–36

    CAS  Google Scholar 

  • Sirhindi G, Mir MA, Abd-Allah EF, Ahmad P, Gucel S (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in Glycine max under nickel toxicity. Front Plant Sci 7:1–12

    Article  Google Scholar 

  • Smolen S, Kowalska I, Czernicka M, Halka M, Keska K, Sady W (2016) Iodine and selenium biofertification with additional application of salicylic acid affects yield, selected molecular parameters and chemical composition of lettuce plants (Lactuca sativa L. var. capitata). Front Plant Sci 7:1–16

    Google Scholar 

  • Sommer AL, Lipman CB (1926) Evidence on the indispensable nature of zinc and boron for higher green plants. Plant Physiol 1:231–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soundararajan P, Manivannan A, Cho YS, Jeong BR (2017) Exogenous supplementation of silicon improved the recovery of hyperhydric shoots in Dianthus caryophyllus L. by stabilizing the physiology and protein expression. Front Plant Sci 8:1–17

    Article  Google Scholar 

  • Sun H, Dai H, Wang X, Wang G (2016) Physiological and proteomic analysis of selenium-mediated tolerance to Cd stress in cucumber (Cucumis sativus L.). Ecotoxicol Environ Saf 133:114–126

    Article  CAS  PubMed  Google Scholar 

  • Takehisa H, Sato Y, Antonio B, Nagamura Y (2015) Coexpression network analysis of macronutrient deficiency response genes in rice. Rice 8:1–7

    Article  Google Scholar 

  • Tamburino R, Vitale M, Ruggiero A, Sassi M, Sannino L, Arena S, Costa A, Batelli G, Zambrano N, Scaloni A, Grillo S, Scotti N (2017) Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.). BMC Plant Biol 17:1–14

    Article  CAS  Google Scholar 

  • Theriault G, Michael P, Nkongolo K (2016) Comprehensive transcriptome analysis of response to nickel stress in white birch (Betula papyrifera). PLoS ONE 11:1–21

    Article  CAS  Google Scholar 

  • Torregrosa VL, Husekova B, Sychrova H (2016) Potassium uptake mediated by Trk1 Is crucial for Candida glabrate growth and fitness. PLoS ONE 11:1–18

    Google Scholar 

  • Tucker MR (1999) Essential plant nutrients: their presence in North Carolina soils and role in plant nutrition, Agronomic division, NCDA & CS bulletin-Agronomic Division, USA, pp. 1–9

  • Varma A, Shrivastava N (2008) The role of plant genomics in biotechnology. In: Doelle HW, DaSilva EJ (eds) Biotechnology, vol VIII, Encyclopedia of Life Support Systems (EOLSS), Eolss Publishers, Oxford, UK, pp. 1–12

  • Visscher AM, Paul AL, Kirst M, Guy CL, Schuerger AC, Ferl RJ (2010) Growth performance and root transcriptome remodeling of Arabidopsis in response to mars-like levels of magnesium sulfate. PLoS ONE 5:1–16

    Article  CAS  Google Scholar 

  • Wang Y, Hu H, Zhu LY, Li XX (2012) Response to nickel in the proteome of the metal accumulator plant Brassica juncea. J Plant Interact 7:230–237

    Article  CAS  Google Scholar 

  • Wang X, Ma X, Wang H, Li B, Clark G, Guo Y, Roux S, Sun D, Tang W (2015) Proteomic study of microsomal proteins reveals a key role for Arabidopsis annexin 1 in mediating heat stress-induced increase in intracellular calcium levels. Mol Cell Proteomics 14:686–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warington K (1937) Boron in agriculture. Nature 140:1016–1016

    Article  CAS  Google Scholar 

  • Wu F, Liu Z, Xu J, Gao S, Lin H, Liu L, Liu Y, Lu Y (2016) Molecular evolution and association of natural variation in ZmARF31 with low phosphorus tolerance in Maize. Front Plant Sci 7:1–14

    CAS  Google Scholar 

  • Yang LT, Lu YB, Zhang Y, Guo P, Chen LS (2016) Proteomic profile of Citrus grandis roots under long-term boron-deficiency revealed by iTRAQ. Trees 30:1057–1071

    Article  CAS  Google Scholar 

  • Yang Y, Wang Q, Chen Q, Yin X, Qian M, Sun X, Yang Y (2017) Genome wide survey indicates diverse physiological roles of the barley (Hordeum vulgare L.) calcium-dependent protein kinase genes. Sci Rep 7:1–14

    Article  Google Scholar 

  • Yildiz M, Terzi H (2016) Proteomic analysis of chromium stress and sulfur deficiency responses in leaves of two canola (Brassica napus L.) cultivars differing in Cr(VI) tolerance. Ecotoxicol Environ Saf 124:255–266

    Article  CAS  PubMed  Google Scholar 

  • Yina Y, Yanga R, Hana Y, Gua Z (2015) Comparative proteomic and physiological analyses reveal the protective effect of exogenous calcium on the germinating soybean response to salt stress. J Proteomics 113:110–126

    Article  CAS  Google Scholar 

  • You X, Yang LT, Lu YB, Li H, Zhang SQ, Chen LA (2014) Proteomic changes of citrus roots in response to long-term manganese toxicity. Trees 28:1383–1399

    Article  CAS  Google Scholar 

  • Yuan W, Zhang D, Song T, Xu F, Lin S, Xu W, Li Q, Zhu Y, Liang J, Zhang J (2017) Arabidopsis plasma membrane H + -ATPase genes AHA2 and AHA7 have distinct and overlapping roles in the modulation of root tip H+ efflux in response to low-phosphorus stress. J Exp Bot 68:1731–1741

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng J, He X, Quan X, Cai S, Han Y, Nadira UA, Zhang G (2015) Identification of the proteins associated with low potassium tolerance in cultivated and Tibetan wild barley. J Proteomics 126:1–11

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Liu H, Tao P, Chen H (2014) Comparative proteomic analyses provide new insights into low phosphorus stress responses in maize leaves. PLoS ONE 9:1–16

    Google Scholar 

  • Zhang H, Xia Y, Chen C, Zhuang K, Song Y, Shen Z (2016a) Analysis of copper binding proteins in rice radicles exposed to excess copper and hydrogen peroxide stress. Front Plant Sci 7:1–15

    Google Scholar 

  • Zhang S, Zhou R, Zhao H, Korpelainen H, Li C (2016b) iTRAQ-based quantitative proteomic analysis gives insight into sexually different metabolic processes of poplars under nitrogen and phosphorus deficiencies. Proteomics 16:614–628

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Chao M, Wang S, Bu J, Tang J, Li F, Wang Q, Zhang B (2016c) Proteome quantification of cotton xylem sap suggests the mechanisms of potassium deficiency-induced changes in plant resistance to environmental stresses. Sci Rep 6:1–15

    Article  CAS  Google Scholar 

  • Zhang H, Wei C, Yang X, Chen H, Yang Y, Mo Y, Li H, Zhang Y, Ma J, Yang J, Zhang X (2017a) Genome-wide identification and expression analysis of calcium-dependent protein kinase and its related kinase gene families in melon (Cucumis melo L.). PLoS ONE 12:1–23

    Google Scholar 

  • Zhang X, Jiang H, Wang H, Cui J, Wang J, Hu J, Guo L, Qian Q, Xue D (2017b) Transcriptome analysis of rice seedling roots in response to potassium deficiency. Sci Rep 7:1–11

    Article  Google Scholar 

  • Zhao S, Zhang ML, Ma TL, Wang Y (2016) Phosphorylation of ARF2 relieves its repression of transcription of the K + transporter gene HAK5 in response to low potassium stress. Plant Cell 28:3005–3019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou CP, Qi YP, You X, Yang LT, Guo P, Ye X, Zhou XX, Ke FJ, Chen LS (2013) Leaf cDNA-AFLP analysis of two citrus species differing in manganese tolerance in response to long-term manganese-toxicity. BMC Genomics 14:1–19

    Article  CAS  Google Scholar 

  • Zhou D, Yang Y, Zhang J, Jiang F, Craft E, Thannhauser TW, Kochian LV, Liu J (2017a) Quantitative iTRAQ proteomics revealed possible roles for antioxidant proteins in sorghum aluminum tolerance. Front Plant Sci 7:1–14

    Article  Google Scholar 

  • Zhou X, Chen S, Wu H, Yang Y, Xu H (2017b) Biochemical and proteomics analyses of antioxidant enzymes reveal the potential stress tolerance in Rhododendron chrysanthum. Pall Biol Direct 12:1–9

    Article  CAS  Google Scholar 

  • Zhu H, Wang H, Zhu Y, Zou J, Zhao FJ, Huang CF (2015) Genome-wide transcriptomic and phylogenetic analyses reveal distinct aluminum-tolerance mechanisms in the aluminum-accumulating species buckwheat (Fagopyrum tataricum). BMC Plant Bio 15:1–13

    Article  CAS  Google Scholar 

  • Zierer W, Hajirezaei MR, Eggert K, Sauer N, Wiren N, Pommerrenig B (2016) Phloem-specific methionine recycling fuels polyamine biosynthesis in a sulfur-dependent manner and promotes flower and seed development. Plant Physiol 170:790–806

    Article  CAS  PubMed  Google Scholar 

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Acknowledgement

The authors like to thank Mrs. Smruti Rout for correcting the English error of the manuscript.

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Authors and Affiliations

  1. Department of Biotechnology, Academy of Management and Information Technology, IID Centre, 67/68, BidyaVihar, Barunei Hills, Khurda, Odisha, 752057, India

    Rout George Kerry & Sushmita Patra

  2. Centre of Advanced Study in Marine Biology, Annamalai University, Parangipettai, Tamilnadu, 608502, India

    Gyana Prakash Mahapatra

  3. Biochemistry and Molecular Biology Laboratory, Post Graduate Department of Botany, Utkal University, VaniVihar, Bhubaneswar, Odisha, 751004, India

    Santi Lata Sahoo & Chinmay Pradhan

  4. School of Biological Sciences, Asian Institute of Public Health, 28A, Unit-VI, Ganganagar, Bhubaneswar, Odisha, 751001, India

    Bijaya Kumar Padhi & Jyoti Ranjan Rout

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  1. Rout George Kerry
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Kerry, R.G., Mahapatra, G.P., Patra, S. et al. Proteomic and genomic responses of plants to nutritional stress. Biometals 31, 161–187 (2018). https://doi.org/10.1007/s10534-018-0083-9

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