Abstract
Aims
Understanding the molecular responses of plant roots to the challenging environment contributes to engineering plants with improved stress tolerance. However, little has been done to understand rice (Oryza sativa L.) roots response to the toxic concentration of zinc (Zn) at the proteomic level. This study explored proteomic responses of young rice roots 5–6 days after sowing to 765 μM of Zn in a hydroponic set-up after 4-day exposure.
Methods
Dye staining method and spectrophotometry were chosen for physiological response investigations. ICP-MS was used to determine metal content in rice seedlings. Two-dimensional gel electrophoresis was used for the proteomic study of root tissue.
Results
Elevated Zn reduced Mg translocation to the shoots and Mn uptake, decreased plant growth, and increased cell death of roots. Zn stimulated the biosynthesis of glutathione but decreased ROS and malondialdehyde levels. In total, 42 Zn-responsive proteins were identified. Proteins involved in redox regulation, defense response, sulfur metabolism, and proteolysis were induced, while those of energy production and cell wall biogenesis were decreased.
Conclusion
Roots of O. sativa seedlings could tolerate certain Zn excess (765 μM Zn for 4 days) by stimulating nutrient recycling and glycolysis, and production of defensive metabolites and proteins to maintain ion and redox homeostasis. Besides, adenosylhomocysteinase (AHCY) down-regulation may contribute to balanced transmethylations, and methionine salvage pathway appears important for the adaptation to Zn. Our results provide some new insight into a complex metabolic response of rice roots to Zn stress, which is related to both stress and defense mechanisms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- LC-MALDI-TOF/TOF MS:
-
liquid chromatography tandem matrix-assisted laser desorption/ionization time-of-flight/time-of-flight mass spectrometry
- 2-DE:
-
two-dimensional gel electrophoresis
- SDS-PAGE :
-
sodium dodecyl sulfate-polyacrylamide gel electrophoresis
- GSH:
-
reduced glutathione
- ROS:
-
reactive oxygen species
- GO:
-
Gene Ontology
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- PPI:
-
protein-protein interaction
- ICP-MS:
-
inductively coupled plasma mass spectrometry
- DAPs :
-
differentially abundant proteins
References
Agrawal GK, Jwa NS, Rakwal R (2009) Rice proteomics: ending phase I and the beginning of phase II. Proteomics 9:935–963. https://doi.org/10.1002/pmic.200800594
Ahmed B, Dwivedi S, Abdin MZ, Azam A, Al-Shaeri M, Khan MS, Saquib Q, Al-Khedhairy AA, Musarrat J (2017) Mitochondrial and chromosomal damage induced by oxidative stress in Zn2+ ions, ZnO-bulk and ZnO-NPs treated Allium cepa roots. Sci Rep 7:40685. https://doi.org/10.1038/srep40685
Andème-Ondzighi C, Christopher DA, Cho EJ, Chang SC, Staehelin LA (2008) Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20:2205–2220. https://doi.org/10.1105/tpc.108.058339
Arenhart RA, Bai Y, Valter De Oliveira LF, Bucker Neto L, Schunemann M, Maraschin FDS, Mariath J, Silverio A, Sachetto-Martins G, Margis R, Wang ZY, Margis-Pinheiro M (2014) New insights into aluminum tolerance in rice: the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol Plant 7:709–721. https://doi.org/10.1093/mp/sst160
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Bassham DC, Clouse S (2017) Developmental cell selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev Cell 41:33–46. https://doi.org/10.1016/j.devcel.2017.03.013
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019. https://doi.org/10.1590/S1415-47572012000600016
Chang HHB, Lin CWC, Huang HJH (2005) Zinc-induced cell death in rice (Oryza sativa L.) roots. Plant Growth Regul 46:261–266. https://doi.org/10.1007/s10725-005-0162-0
Chen J, Xiao Q, Wu F, Dong X, He J, Pei Z, Zheng H (2010) Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol 30:1570–1585. https://doi.org/10.1093/treephys/tpq086
Chen J, Wu F-H, Wang W-H, Zheng C-J, Lin G-H, Dong X-J, He J-X, Pei Z-M, Zheng H-L (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493. https://doi.org/10.1093/jxb/err145
Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318. https://doi.org/10.1007/s11104-012-1275-7
Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li H, Jinn TL (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139:425–436. https://doi.org/10.1104/pp.105.065284
De Souza Silva ML, Vitti GC, Trevizam AR (2014) Heavy metal toxicity in rice and soybean plants cultivated in contaminated soil. Rev Ceres 61:248–254. https://doi.org/10.1590/S0034-737X2014000200013
Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P, Bennett M, Mansfield J, Zipfel C, Hamann T (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol 156:1364–1374. https://doi.org/10.1104/pp.111.175737
Ding Y, Luo W, Xu G (2006) Characterisation of magnesium nutrition and interaction of magnesium and potassium in rice. Ann Appl Biol 149:111–123. https://doi.org/10.1111/j.1744-7348.2006.00080.x
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. https://doi.org/10.1093/nar/gkq310
Fageria NK, dos Santos AB, Cobucci T (2011) Zinc nutrition of lowland rice. Commun Soil Sci Plant Anal 42:1719–1727. https://doi.org/10.1080/00103624.2011.584591
Famoso AN, Clark RT, Shaff JE, Craft E, McCouch SR, Kochian LV (2010) Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol 153:1678–1691. https://doi.org/10.1104/pp.110.156794
Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446. https://doi.org/10.1038/nature01485
Fujii S, Kazama T, Ito Y, Kojima S, Toriyama K (2014) A candidate factor that interacts with RF2, a restorer of fertility of Lead rice-type cytoplasmic male sterility in rice. Rice 7:21. https://doi.org/10.1186/s12284-014-0021-6
Glińska S, Gapińska M, Michlewska S, Skiba E, Kubicki J (2016) Analysis of Triticum aestivum seedling response to the excess of zinc. Protoplasma 253:367–377. https://doi.org/10.1007/s00709-015-0816-3
Gu HH, Zhan SS, Wang SZ, Tang YT, Chaney RL, Fang XH, De Cai X, Qiu RL (2012) Silicon-mediated amelioration of zinc toxicity in rice (Oryza sativa L.) seedlings. Plant Soil 350:193–204. https://doi.org/10.1007/s11104-011-0894-8
Hajduch M, Rakwal R, Agrawal GK, Yonekura M, Pretova A (2001) High-resolution two-dimensional electrophoresis separation of proteins from metal-stressed rice (Oryza sativa L.) leaves: drastic reductions/ fragmentation of ribulose-1,5-bisphosphate carboxylase/oxygenase and induction of stress-related proteins. Electrophoresis 22:2824–2831. https://doi.org/10.1002/1522-2683(200108)22:13<2824::AID-ELPS2824>3.0.CO;2-C
Hameed SMS, Sarma SP (2011) The Structure of the Thioredoxin–Triosephosphate Isomerase Complex Provides Insights into the Reversible Glutathione-Mediated Regulation of Triosephosphate Isomerase. Biochemistry 51(1):533–544
Han X, Wang Y, Liu X, Jiang L, Ren Y, Liu F, Peng C, Li J, Jin X, Wu F, Wang J, Guo X, Zhang X, Cheng Z, Wan J (2012) The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice. J Exp Bot 63:121–130. https://doi.org/10.1093/jxb/err262
Herren T, Feller U (1997) Influence of increased zinc levels on phloem transport in wheat shoots. J Plant Physiol 150:228–231. https://doi.org/10.1016/S0176-1617(97)80208-8
Hirose T, Scofield GN, Terao T (2008) An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci 174:534–543. https://doi.org/10.1016/j.plantsci.2008.02.009
Hoepflinger MC, Reitsamer J, Geretschlaeger AM, Mehlmer N, Tenhaken R (2013) The effect of translationally controlled tumour protein (TCTP) on programmed cell death in plants. BMC Plant Biol 13:135. https://doi.org/10.1186/1471-2229-13-135
Hu T, Yang J, Wu X, Huang X, Chen Z, Wu Y (2013) Overexpression of a specific OsGSTL2 isoenzyme improves glyphosate and chlorsulfuron tolerance of transgenic rice plants. Afr J Agric Res 8:1520–1527. https://doi.org/10.5897/AJAR12.868
Hu WJ, Chen J, Liu TW, Simon M, Wang WH, Chen J, Wu FH, Liu X, Shen ZJ, Zheng HL (2014) Comparative proteomic analysis of differential responses of Pinus massoniana and Taxus wallichiana var. mairei to simulated acid rain. Int J Mol Sci 15:4333–4355. https://doi.org/10.3390/ijms15034333
Ishimaru Y, Suzuki M, Ogo Y, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2008) Synthesis of nicotianamine and deoxymugineic acid is regulated by OsIRO2 in Zn excess rice plants. Soil Sci Plant Nutr 54:417–423. https://doi.org/10.1111/j.1747-0765.2008.00259.x
Ishimaru Y, Bashir K, Nishizawa NK (2011) Zn uptake and translocation in rice plants. Rice 4:21–27. https://doi.org/10.1007/s12284-011-9061-3
Kim SG, Kim ST, Wang Y, Yu S, Choi IS, Kim YC, Kim WT, Agrawal GK, Rakwal R, Kang KY (2011) The RNase activity of rice probenazole-induced protein1 (PBZ1) plays a key role in cell death in plants. Mol Cells 31(1):25–31
Kim YJ, Yeu SY, Park BS, Koh HJ, Song JT, Seo HS (2012) Protein disulfide isomerase-like protein 1-1 controls endosperm development through regulation of the amount and composition of seed proteins in rice. PLoS One 7:e44493. https://doi.org/10.1371/journal.pone.0044493
Kosová K, Vítámvás P, Prášil IT (2014) Proteomics of stress responses in wheat and barley—search for potential protein markers of stress tolerance. Front Plant Sci 5:1–14. https://doi.org/10.3389/fpls.2014.00711
Kumar G, Kushwaha HR, Panjabi-Sabharwal V, Kumari S, Joshi R, Karan R, Mittal S, Singla-Pareek SL, Pareek A (2012) Clustered metallothionein genes are co-regulated in rice and ectopic expression of OsMT1e-P confers multiple abiotic stress tolerance in tobacco via ROS scavenging. BMC Plant Biol 12:107. https://doi.org/10.1186/1471-2229-12-107
Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Expression of a rice lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. J Hazard Mater 248–249:228–237. https://doi.org/10.1016/j.jhazmat.2013.01.004
Lam PY, Tobimatsu Y, Takeda Y, Suzuki S, Yamamura M, Umezawa T, LoC (2017) Disrupting Flavone Synthase II Alters Lignin and Improves Biomass Digestibility. Plant Physiol 174(2):972–985
Lan HX, Wang ZF, Wang QH, Wang MM, Bao YM, Huang J, Zhang HS (2013) Characterization of a vacuolar zinc transporter OZT1 in rice (Oryza sativa L.). Mol Biol Rep 40:1201–1210. https://doi.org/10.1007/s11033-012-2162-2
Li N, Zhang DS, Liu HS, Yin CS, Li X, Liang W, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014. https://doi.org/10.1105/tpc.106.044107
Li X, Chen W, Zhao Y, Xiang Y, Jiang H, Zhu S, Cheng B (2013) Downregulation of caffeoyl-CoA O-methyltransferase (CCoAOMT) by RNA interference leads to reduced lignin production in maize straw. Genet Mol Biol 36:540–546. https://doi.org/10.1590/S1415-47572013005000039
Liu L, Zhou Y, Zhou G, Ye R, Zhao L, Li X, Lin Y (2008) Identification of early senescence-associated genes in rice flag leaves. Plant Mol Biol 67:37–55. https://doi.org/10.1007/s11103-008-9300-1
Liu J, Cao C, Wong M, Zhang Z, Chai Y (2010) Variations between rice cultivars in iron and manganese plaque on roots and the relation with plant cadmium uptake. J Environ Sci 22:1067–1072. https://doi.org/10.1016/S1001-0742(09)60218-7
Liu TW, Fu B, Niu L, Chen J, Wang WH, He JX, Pei ZM, Zheng HL (2011) Comparative proteomic analysis of proteins in response to simulated acid rain in Arabidopsis. J Proteome Res 10:2579–2589. https://doi.org/10.1021/pr200056a
Liu H, Soomro A, Zhu Y, Qiu X, Chen K, Zheng T, Yang L, Xing D, Xu J (2016a) QTL underlying iron and zinc toxicity tolerances at seedling stage revealed by two sets of reciprocal introgression populations of rice (Oryza sativa L.). Crop J 4:280–289. https://doi.org/10.1016/j.cj.2016.05.007
Liu X, Chen J, Wang GH, Wang WH, Shen ZJ, Luo MR, Gao GF, Simon M, Ghoto K, Zheng HL (2016b) Hydrogen sulfide alleviates zinc toxicity by reducing zinc uptake and regulating genes expression of antioxidative enzymes and metallothioneins in roots of the cadmium/zinc hyperaccumulator Solanum nigrum L. Plant Soil 400:177–192. https://doi.org/10.1007/s11104-015-2719-7
Lock K, Janssen C (2003) Influence of ageing on zinc bioavailability in soils. Environ Pollut 126:371–374. https://doi.org/10.1016/S0269-7491(03)00232-X
Marchand CH, Vanacker H, Collin V, Issakidis-Bourguet E, Le Maréchal P, Decottignies P (2010) Thioredoxin targets in Arabidopsis roots. Proteomics 10:2418–2428. https://doi.org/10.1002/pmic.200900835
Mehrabanjoubani P, Abdolzadeh A, Sadeghipour HR, Aghdasi M (2015) Impacts of silicon nutrition on growth and nutrient status of rice plants grown under varying zinc regimes. Theor Exp Plant Physiol 27:19–29. https://doi.org/10.1007/s40626-014-0028-9
Meng L, Wang B, Zhao X, Ponce K, Qian Q, Ye G (2017) Association mapping of ferrous, zinc, and aluminum tolerance at the seedling stage in indica rice using MAGIC populations. Front Plant Sci 8:159–176. https://doi.org/10.3389/fpls.2017.01822
Menguer PK, Farthing E, Peaston KA, Ricachenevsky FK, Fett JP, Williams LE (2013) Functional analysis of the rice vacuolar zinc transporter OsMTP1. J Exp Bot 64:2871–2883. https://doi.org/10.1093/jxb/ert136
Miljuš-Djukić J, Stanisavljević N, Radović S, Jovanović Ž, Mikić A, Maksimović V (2013) Differential response of three contrasting pea (Pisum arvense, P. Sativum and P. Fulvum) species to salt stress: assessment of variation in antioxidative defence and miRNA expression. Aust J Crop Sci 7:2145–2153 http://biore.bio.bg.ac.rs/handle/123456789/2683
Moffatt BA, Weretilnyk EA (2001) Sustaining S-adenosyl-L-methionine-dependent methyltransferase activity in plant cells. Physiol Plant 113:435–442. https://doi.org/10.1034/j.1399-3054.2001.1130401.x
Muschitz A, Faugeron C, Morvan H (2009) Response of cultured tomato cells subjected to excess zinc: role of cell wall in zinc compartmentation. Acta Physiol Plant 31:1197–1204. https://doi.org/10.1007/s11738-009-0354-8
Nag P, Nag P, Paul AK, Mukherji S (1984) Toxic action of zinc on growth and enzyme activities of rice Oryza sativa L. seedlings. Environ Pollut Ser a. Ecol Biol 36:45–59. https://doi.org/10.1016/0143-1471(84)90197-1
Onda Y, Kobori Y (2014) Differential activity of rice protein disulfide isomerase family members for disulfide bond formation and reduction. FEBS Open Bio 4:730–734. https://doi.org/10.1016/j.fob.2014.07.007
Rahman A, Hossain MS, Mahmud J-A, Nahar K, Hasanuzzaman M, Fujita M (2016) Manganese-induced salt stress tolerance in rice seedlings: regulation of ion homeostasis, antioxidant defense and glyoxalase systems. Physiol Mol Biol Plants 22:291–306. https://doi.org/10.1007/s12298-016-0371-1
Romero LC, Aroca MÁ, Laureano-Marín AM, Moreno I, García I, Gotor C (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant 7:264–276. https://doi.org/10.1093/mp/sst168
Ros R, Muñoz-Bertomeu J, Krueger S (2014) Serine in plants: biosynthesis, metabolism, and functions. Trends Plant Sci 19:564–569. https://doi.org/10.1016/j.tplants.2014.06.003
Sade N, del Mar R-WM, Umnajkitikorn K, Blumwald E (2018) Stress-induced senescence and plant tolerance to abiotic stress. J Exp Bot 69:845–853. https://doi.org/10.1093/jxb/erx235
Sadeghzadeh B, Rengel Z (2011) Zinc in soils and crop nutrition. In: Hawkesford MJ, Barraclough P (eds) The molecular and physiological basis of nutrient use efficiency in crops. Wiley-Blackwell, Oxford, pp 335–375
Sahoo RK, Ansari MW, Tuteja R, Tuteja N, Acquaah G, Chen J, Du X, Zhao H, Zhou X, Egamberdieva D, Harrison M, Kuppu S, Mishra N, Hu R, Sun L, Zhu X, Shen G, Blumwald E, Payton P, Zhang H, Mahajan S, Tuteja N, Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran L, Qin F, Kodaira K, Maruyama K, Mizoi J, Tran L, Fujita Y, Morimoto K, Shinozaki K, Yamaguchi-Shinozaki K, Sahoo R, Tuteja N, Tuteja N, Sahoo R, Garg B, Tuteja R, Tuteja N, Zolla G, Heimer Y, Barak S (2014) OsSUV3 transgenic rice maintains higher endogenous levels of plant hormones that mitigates adverse effects of salinity and sustains crop productivity. Rice 7:17. https://doi.org/10.1186/s12284-014-0017-2
Sauter M, Moffatt B, Saechao MC, Hell R, Wirtz M (2013) Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. Biochem J 451:145–154. https://doi.org/10.1042/BJ20121744
Seo DH, Seomun S, Do CY, Jang G (2020) Root development and stress tolerance in rice: the key to improving stress tolerance without yield penalties. Int J Mol Sci 21:1807. https://doi.org/10.3390/ijms21051807
Shannon P (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Simmons RW, Pongsakul P, Saiyasitpanich D, Klinphoklap S (2005) Elevated levels of cadmium and zinc in paddy soils and elevated levels of cadmium in rice grain downstream of a zinc mineralized area in Thailand: implications for public health. Environ Geochem Health 27:501–511. https://doi.org/10.1007/s10653-005-7857-z
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. https://doi.org/10.3389/fpls.2016.00591
Song A, Li P, Li Z, Fan F, Nikolic M, Liang Y (2011) The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. Plant Soil 344:319–333. https://doi.org/10.1007/s11104-011-0749-3
Song A, Li P, Fan F, Li Z, Liang Y (2014) The effect of silicon on photosynthesis and expression of its relevant genes in rice (Oryza sativa L.) under high-zinc stress. PLoS One 9:e113782. https://doi.org/10.1371/journal.pone.0113782
Stein O, Secchi F, German MA, Damari-Weissler H, Aloni R, Holbrook NM, Zwieniecky MA, Granot D (2018) The tomato cytosolic fructokinase FRK1 is important for phloem fiber development. Biol Plant 62:353–361. https://doi.org/10.1007/s10535-017-0762-3
Stephan CH, Courchesne F, Hendershot WH, McGrath SP, Chaudri AM, Sappin-Didier V, Sauvé S (2008) Speciation of zinc in contaminated soils. Environ Pollut 155:208–216. https://doi.org/10.1016/j.envpol.2007.12.006
Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6:e21800. https://doi.org/10.1371/journal.pone.0021800
Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H (2012) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607. https://doi.org/10.4161/psb.22454
Tao J-J, Cao Y-R, Chen H-W, Wei W, Li Q-T, Ma B, Zhang W-K, Chen S-Y, Zhang J-S (2015) Tobacco translationally controlled tumor protein interacts with ethylene receptor tobacco histidine kinase1 and enhances plant growth through promotion of cell proliferation. Plant Physiol 169:96–114. https://doi.org/10.1104/pp.15.00355
Tennstedt P, Peisker D, Bottcher C, Trampczynska A, Clemens S, Böttcher C, Trampczynska A, Clemens S (2008) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149:938–948. https://doi.org/10.1104/pp.108.127472
Thao NP, Khan MIR, Thu NBA, Hoang XLT, Asgher M, Khan NA, Tran LSP (2015) Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress. Plant Physiol 169:73–84. https://doi.org/10.1104/pp.15.00663
The Inkscape Team (2019). Inkscape 0.92.4 (5da689c313, 2019-01-14). https://inkscape.org/
Tsednee M, Yang SC, Lee DC, Yeh KC (2014) Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability. Plant Physiol 166:839–852. https://doi.org/10.1104/pp.114.241224
Tuteja N, Sahoo RK, Garg B, Tuteja R (2013) OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64). Plant J 76:115–127. https://doi.org/10.1111/tpj.12277
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688. https://doi.org/10.1093/jxb/erp119
Van De Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Ver E, Van Themaat L, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147. https://doi.org/10.1104/pp.106.082073
Vandereyken K, Van Leene J, De Coninck B, Cammue BPA (2018) Hub protein controversy: taking a closer look at plant stress response hubs. Front Plant Sci 9:694. https://doi.org/10.3389/fpls.2018.00694
Wahyudi A, Ariyani D, Ma G, Inaba R, Fukasawa C, Nakano R, Motohashi R (2018) Functional analyses of lipocalin proteins in tomato. Plant Biotechnol 35:303–312. https://doi.org/10.5511/plantbiotechnology.18.0620a
Walsh TA, Green SB, Larrinua IM, Schmitzer PR (2001) Characterization of plant β-ureidopropionase and functional overexpression in Escherichia coli. Plant Physiol 125:1001–1011. https://doi.org/10.1104/pp.125.2.1001
Wang Y, Yu Y, Huang M, Gao P, Chen H, Liu M, Chen Q, Yang Z, Sun Q (2020) Transcriptomic and proteomic profiles of II YOU 838 (Oryza sativa) provide insights into heat stress tolerance in hybrid rice. PeerJ 8:e8306. https://doi.org/10.7717/peerj.8306
Wei Y, Bai Y, Jin J, Yang L, Yao Z, Xu S, Luo G, Song W, Zhu C (2007) Sufficiency and deficiency indices of soil available zinc for Rice in the alluvial soil of the coastal Yellow Sea. Rice Sci 14:223–228. https://doi.org/10.1016/S1672-6308(07)60031-6
Wu J, Wang C, Zheng L, Wang L, Chen Y, Whelan J, Shou H (2011) Ethylene is involved in the regulation of iron homeostasis by regulating the expression of iron-acquisition-related genes in Oryza sativa. J Exp Bot 62:667–674. https://doi.org/10.1093/jxb/erq301
Wu X, Xiong E, Wang W, Scali M, Cresti M (2014) Universal sample preparation method integrating trichloroacetic acid/acetone precipitation with phenol extraction for crop proteomic analysis. Nat Protoc 9:362–374. https://doi.org/10.1038/nprot.2014.022
Xia K, Zeng X, Jiao Z, Li M, Xu W, Nong Q, Mo H, Cheng T, Zhang M (2018) Formation of protein disulfide bonds catalyzed by OsPDIL1;1 is mediated by microRNA5144-3p in rice. Plant Cell Physiol 59:331–342. https://doi.org/10.1093/pcp/pcx189
Yu CS, Cheng CW, Su WC, Chang KC, Huang SW, Hwang JK, Lu CH (2014) CELLO2GO: a web server for protein subcellular localization prediction with functional gene ontology annotation. PLoS One 9:e99368. https://doi.org/10.1371/journal.pone.0099368
Zhang Y, Chen K, Zhao F, Sun C, Jin C, Shi Y, Sun Y, Li Y, Yang M, Jing X, Luo J, Lian X (2018) OsATX1 interacts with heavy metal P1B-type ATPases and affects copper transport and distribution. Plant Physiol 178:329–344. https://doi.org/10.1104/pp.18.00425
Zhang HH, Xu N, Teng ZY, Wang JR, Ma S, Wu X, Li X, Sun GY (2019) 2-Cys Prx plays a critical role in scavenging H2O2 and protecting photosynthetic function in leaves of tobacco seedlings under drought stress. J Plant Interact 14:119–128. https://doi.org/10.1080/17429145.2018.1562111
Acknowledgments
This work was financially supported by the National Key Research and Development Program of China (2017YFC0506102), the Natural Science Foundation of China (NSFC) (31870581, 31570586 and 31601133), the project of Inter-governmental Science & Technology Cooperation between P.R. China and Slovenia awarded by Ministry of Science and Technology of the P.R of China (2014-140-10-6) and Slovenian Research Agency (BI-CN/14-15-006), the Chinese Government Scholarship to study in China awarded by Chinese Scholarship Council, and the Ad Futura Scholarship from Public Scholarship, Development, Disability and Maintenance Fund of the Republic of Slovenia (11010-498/2012-28). We appreciate anonymous reviewers and editor for the insightful comments and valuable suggestions.
Author information
Authors and Affiliations
Contributions
Martin Šimon: Conceptualization, Investigation, Formal analysis, Writing - Original Draft, Writing - Review & Editing. Zhi-Jun Shen: Methodology, Validation, Investigation. Kabir Ghoto: Investigation, Resources. Juan Chen: Conceptualization, Methodology, Validation, Investigation. Xiang Liu: Conceptualization, Methodology, Validation, Investigation. Gui-Feng Gao: Conceptualization. Anita Jemec Kokalj: Writing - Review & Editing. Sara Novak: Writing - Review & Editing. Barbara Drašler: Writing - Review & Editing. Jing-Ya Zhang: Resources. Yan-Ping You: Resources. Damjana Drobne: Supervision, Writing - Review & Editing. Hai-Lei Zheng: Conceptualization, Supervision, Writing - Review & Editing.
Corresponding authors
Ethics declarations
Competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Responsible Editor: Miroslav Nikolic.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOC 4997 kb)
Rights and permissions
About this article
Cite this article
Šimon, M., Shen, ZJ., Ghoto, K. et al. Proteomic investigation of Zn-challenged rice roots reveals adverse effects and root physiological adaptation. Plant Soil 460, 69–88 (2021). https://doi.org/10.1007/s11104-020-04772-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04772-1