Abstract
Background and aims
Mechanisms by which soil pH affects rice growth await further elucidation.
Methods
We have used a Systems Biology approach to elucidate the nature of the damage caused by extreme pH to plant growth and iron homeostasis, and the adaptive plant responses elicited.
Results
Optimum pH for rice growth was pH 6. Comparative transcriptome analysis revealed that 83% of 1318 DEGs were down-regulated at pH 4, while 73% among of 1168 DEGs were up-regulated at pH 8. GO enrichment analysis showed significant enhancement of oxidation-reduction and oxidative stress responses. Environmental pH regulated cellular oxidation-reduction processes and metabolic pathways controlling rice growth. Additionally, pH affected cellular iron-homeostasis by regulating root apoplastic iron deposition. Low pH enhanced iron mobilization from root apoplast and accumulation in plant tissues, and down-regulated iron transport related genes to prevent iron toxicity. Conversely,high pH induced blockage of iron mobilization from root apoplast. Rhizosphere pH affected aerenchyma formation and exodermis-apoplastic barriers under control of ROS, already weakened and enhanced by low pH and high pH, respectively.
Conclusions
ROS-mediated redox signaling plays an important role in regulating rice growth under varying pH conditions. Cellular iron homeostasis was disturbed through regulation of iron plaque formation and apoplastic iron mobilization in rice roots under acidic and alkaline conditions.
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References
Aloni R, Enstone DE, Peterson CA (1998) Indirect evidence for bulk water flow in root cortical cell walls of three dicotyledonous species. Planta 207:1–7
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106
Becker M, Asch F (2005) Iron toxicity in rice-conditions and management concepts. J Soil Sci Plant Nutr 168:558–573
Chen H, Zhang Q, Cai H, Xu F (2017). Ethylene mediates alkaline-induced rice growth inhibition by negatively regulating plasma membrane H+-ATPase activity in roots. Front Plant Sci 8: 1839
Chen H, Zhang Q, Cai H, Zhou W, Xu F (2018) H2O2 mediates nitrate-induced iron chlorosis by regulating iron homeostasis in rice. Plant Cell Environ 41:767–781
Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127
Enstone DE, Peterson CA, Ma F (2002) Root endodermis and exodermis: structure, function. and responses to the environment J Plant Growth Regul 21:335–351
Evans DE (2003) Aerenchyma formation. New Phytol 161:35–49
Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen K (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KW, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010
Harrison PM, Arosio P (1996) The ferritins: molecular properties, iron storage function and cellular regulation. BBA-Bioenergetics 1275:161–203
Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59
Ideker T, Galitski T, Hood L (2001) A new approach to decoding life: systems biology. Annu Rev Genom Hum G 2:343–372
Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y, Sato Y, Nishizawa NK (2011) A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286: 24649-24655
Ishimaru Y, Kim S, Tsukamoto T, Oki H, Kobayashi T, Watanabe S, Nishizawa NK (2007) Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. PNAS 104:7373–7378
Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Kobayashi Y, Ikka T, Hirayama T, Shinozaki K, Kobayashi M (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. PNAS 104:9900–9905
Jin CW, You GY, He YF, Tang C, Wu P, Zheng SJ (2007) Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144: 278-285
Kobayashi T, Ogo Y, Itai RN, Nakanishi H, Takahashi M, Mori S, Nishizawa NK (2007) The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. PNAS 104:19150–19155
Kobayashi Y, Kobayashi Y, Watanabe T, Shaff JE, ohta H, Kochian LV, Wagatsuma T, Kinraide TB, Koyama H (2013) Molecular and physiological analysis of Al3+ and H+ rhizotoxicities at moderately acidic conditions. Plant Physiol 163:180–192
Kochian LV, Pineros MA, Liu JP, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598
Kosegarten HU, Hoffmann B, Mengel K (1999) Apoplastic pH and Fe3+ reduction in intact sunflower leaves. Plant Physiol 121:1069–1079
Kosegarten HU, Hoffmann B, Mengel K (2001) The paramount influence of nitrate inincreasing apoplastic pH of young sunflower leaves to induce Fe deficiency chlorosis, and the re-greening effect brought about by acidic foliar sprays. J Plant Nutr Soil Sc 164:155–163
Koyama H, toda T, Hara T (2001) Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana, pectin-ca interaction may play an important role in proton rhizotoxicity. J Exp Bot 52:361–368
Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153:402–412
Li Q, Yang A, Zhang WH (2016) Efficient acquisition of iron confers greater tolerance to saline-alkaline stress in rice (Oryza sativa L.). J Exp Bot 67: 6431–6444
Liu J, Guo Y (2011) The alkaline tolerance in Arabidopsis requires microfilament partially through inactivation of PKS5 kinase. J Genet Genomics 38:307–313
Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, Ding Z (2018) Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genet 14:e1007144
Mengel K (1994) Iron availability in plant tissues-iron chlorosis on calcareous soils. Plant Soil 165:275–283
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309
Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N (2012) Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. PNAS 109:10101–10106
Nikolic M, Römheld V (2003) Nitrate does not result in iron inactivation in the apoplast of sunflower leaves. Plant Physiol 132:1303–1314
Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454
Ogo Y, Kobayashi T, Itai RN, Nakanishi H, Kakei Y, Takahashi M, Nishizawa NK (2008) A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem 283:13407–13417
Ogo Y, Itai RN, Kobayashi T, Aung MS, Nakanishi H, Nishizawa NK (2011) OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Mol Biol 75:593–605
Orman-Ligeza B, Parizot B, de Rycke R, Fernandez A, Himschoot E, Van Breusegem F (2016) RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development: dev.136465
Pärtel M (2002) Local plant diversity patterns and evolutionary history at the regional scale. Ecology 83:2361–2366
Peterson CA, Perumalla CJ (1990) A survey of angiosperm species to detect hypodermal Casparian bands. II. Roots with a multiseriate hypodermis or epidermis. Boi J Linn Soc 103: 113-125
Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697
Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149:167–192
Schreiber L (2010) Transport barriers made of cutin. suberin and associated waxes Trends Plant Sci 15:546–553
Slessarev EW, Lin Y, Bingham NL, Johnson JE, Dai Y, Schimel JP, Chadwick OA (2016) Water balance creates a threshold in soil pH at the global scale. Nature 540:567–569
Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C, Lin X (2015) Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integr Plant Biol 57:550–561
Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466–469
Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616
von Wiren N, Klair S, Bansal S, Briat JF, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol 119:1107–1114
Wang LU, Ying Y, Narsai R, Ye L, Zheng L, Tian J, Shou H (2013) Identification of OsbHLH133 as a regulator of iron distribution between roots and shoots in Oryza sativa. Plant Cell Environ 36:224–236
Wu L, Shhadi M, Gregorio G, Matthus E, Becker M, Frei M (2014) Genetic and physiological analysis of tolerance to acute iron toxicity in rice. Rice 7:1–12
Yamauchi T, Shiono K, Nagano M, Fukazawa A, Ando M, Takamure I, Mori H, Nishizawa NK, Kawai-Yamada M, Tsutsumi N, Kato K, Nakazono M (2015) Ethylene biosynthesis is promoted by very-long-chain fatty acids during ly-sigenous aerenchyma formation in rice roots. Plant Physiol 169:180–193
Yamauchi T, Yoshioka M, Fukazawa A, Mori H, Nishizawa NK, Tsutsumi N, Nakazono M (2017) An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell 29:775–790
Yan F, Schubert S, Mengel K (1992) Effect of low root medium pH on net proton release, root respiration, and root growth of corn (Zea mays L.) and broad bean (Vicia faba L.). Plant Physiol 99: 415–421
Yu XL, Wu DM, Fu YQ, Xu JY, Baluška F, Shen H (2018) OsGLO4 is involved in the formation of iron plaques on surface of rice roots grown under alternative wetting and drying condition. Plant Soil 423:111–123
Zhalnina K, Dias R, de Quadros PD, Davis-Richardson A, Camargo FA, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–406
Zhang JT, Mu CS (2009) Effects of saline and alkaline stresses on the germination, growth, photosynthesis, ionic balance and antioxidant system in an alkali-tolerant leguminous forage Lathyrus quinquenervius. J Plant Nutr Soil Sc 55:685–697
Zheng L, Ying Y, Wang L, Wang F, Whelan J, Shou H (2010) Identification of a novel iron regulated basic helix-loop-helix protein involved in Fe homeostasis in Oryza sativa. BMC Plant Biol 10:166
Acknowledgements
This study was financially supported in part by the Province Key R&D Program of Hunan (2018NK1010); National Key R&D Program of China (2017YFD0200100, 2017YFD0200103); National Natural Science Foundation of China (Grant No.31101596, 31372130); Hunan Provincial Recruitment Program of Foreign Experts; and the National Oilseed Rape Production Technology System of China; “2011 Plan” supported by The Chinese Ministry of Education; Research and Innovation Project of postgraduates in Hunan province (CX2015B242), Double First-class Construction Project of Hunan Agricultural University (kxk201801005).
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Chen, H., Zhang, Q. & Zhang, Z. Comparative transcriptome combined with metabolomic and physiological analyses revealed ROS-mediated redox signaling affecting rice growth and cellular iron homeostasis under varying pH conditions. Plant Soil 434, 343–361 (2019). https://doi.org/10.1007/s11104-018-3859-3
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DOI: https://doi.org/10.1007/s11104-018-3859-3