Abstract
Plant iron (Fe) deficiency is widely present in alkaline calcium soils worldwide, and endophytes show great potential for promoting plant nutrient absorption. However, the underlying mechanisms remain unclear. To clarify the mechanisms by which the endophytic fungus Phomopsis liquidambaris promotes peanut Fe absorption, we designed this study to detect the physiological changes in peanut with P. liquidambaris infection. We measured ethylene and auxin in peanuts under Fe deficiency and found that fungal colonization promoted their accumulation (50% and 20%, respectively, at the top point). Moreover, plant Fe absorption ability and transfer were enhanced according to qPCR and enzyme results; the Fe content in the leaf increased (29.52%) as the symptoms of leaf chlorosis were ameliorated. Finally, the chlorophyll content increased (29%), and plant growth was enhanced (13.3%). We also proved that during Fe insufficiency, auxin functions downstream of ethylene to induce the upregulation of Fe absorption-related gene and enzyme activity including that of AHA4, IRT1, H+-ATPase, and FCR. We conclude that the addition of P. liquidambaris activates the auxin signaling pathway downstream of ethylene and improves peanut Fe absorption by promoting rhizosphere acidification, increasing FCR and IRT1 expression in peanut roots, leading to plant Fe absorption and growth.
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References
Angulo M, Garcia MJ, Alcantara E, Perez-Vicente R, Romera FJ (2021) Comparative study of several Fe deficiency responses in the Arabidopsis thaliana ethylene insensitive mutants ein2–1 and ein2–5. Plants-Basel 10(2):262. https://doi.org/10.3390/plants10020262
Bacaicoa E, Mora V, Zamarreno AM, Fuentes M, Casanova E, Garcia-Mina JM (2011) Auxin: a major player in the shoot-to-root regulation of root Fe-stress physiological responses to Fe deficiency in cucumber plants. Plant Physiol Biochem 49(5):545–556. https://doi.org/10.1016/j.plaphy.2011.02.018
Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65:125–153. https://doi.org/10.1146/annurev-arplant-050213-035759
Benson HP, LeVier K, Guerinot ML (2004) A dominant-negative fur mutation in Bradyrhizobium japonicum. J Bacteriol 186(5):1409–1414. https://doi.org/10.1128/JB.186.5.1409-1414.2004
Beyer EM (1976) A potent inhibitor of ethylene action in plants. Plant Physiol 58(3):268–271. https://doi.org/10.1104/pp.58.3.268
Bonku R, Yu JM (2020) Health aspects of peanuts as an outcome of its chemical composition. Food Sci Human Wellness 9(1):21–30. https://doi.org/10.1016/j.fshw.2019.12.005
Celletti S, Pii Y, Valentinuzzi F, Tiziani R, Fontanella MC, Beone GM et al (2020) Physiological responses to fe deficiency in split-root tomato plants: possible roles of auxin and ethylene? Agronomy-Basel 10(7):1000. https://doi.org/10.3390/agronomy10071000
Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T et al (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis. Plant Physiol 154(2):810–819. https://doi.org/10.1104/pp.110.161109
Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol 116(3):1063–1072. https://doi.org/10.1104/pp.116.3.1063
Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409(6818):346–349. https://doi.org/10.1038/35053080
Eroglu S, Meier B, von Wiren N, Peiter E (2016) The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. Plant Physiol 170(2):1030–1045. https://doi.org/10.1104/pp.15.01194
Gao L, Shi YX (2007) Genetic differences in resistance to iron deficiency chlorosis in peanut. J Plant Nutr 30(1):37–52. https://doi.org/10.1080/01904160601054965
Garcia MJ, Lucena C, Romera FJ, Alcantara E, Perez-Vicente R (2010) Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J Exp Bot 61(14):3885–3899. https://doi.org/10.1093/jxb/erq203
Gonzalez-Mas N, Gutierrez-Sanchez F, Sanchez-Ortiz A, Grandi L, Turlings TCJ, Manuel Munoz-Redondo J et al (2021) Endophytic colonization by the entomopathogenic fungus Beauveria Bassiana affects plant volatile emissions in the presence or absence of chewing and sap-sucking insects. Front Plant Sci 12:660460. https://doi.org/10.3389/fpls.2021.660460
Harbort CJ, Hashimoto M, Inoue H, Niu Y, Guan R, Rombola AD et al (2020) Root-secreted coumarins and the microbiota interact to improve iron nutrition in Arabidopsis. Cell Host Microbe 28(6):825–837826. https://doi.org/10.1016/j.chom.2020.09.006
Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agric Exp Station 347:32
Kabir AH, Debnath T, Das U, Prity SA, Haque A, Rahman MM et al (2020) Arbuscular mycorrhizal fungi alleviate Fe-deficiency symptoms in sunflower by increasing iron uptake and its availability along with antioxidant defense. Plant Physiol Biochem 150:254–262. https://doi.org/10.1016/j.plaphy.2020.03.010
Kabir AH, Tahura S, Elseehy MM, El-Shehawi AM (2021) Molecular characterization of Fe-acquisition genes causing decreased Fe uptake and photosynthetic inefficiency in Fe-deficient sunflower. Sci Rep 11(1):5537. https://doi.org/10.1038/s41598-021-85147-z
Kobayashi T, Nozoye T, Nishizawa NK (2019) Iron transport and its regulation in plants. Free Radic Biol Med 133:11–20. https://doi.org/10.1016/j.freeradbiomed.2018.10.439
Liu KD, Yue RQ, Yuan CC, Liu JX, Zhang L, Sun T et al (2015) Auxin signaling is involved in iron deficiency-induced photosynthetic inhibition and shoot growth defect in rice (Oryza sativa L.). J Plant Biol 58(6):391–401. https://doi.org/10.1007/s12374-015-0379-z
Liu M, Zhang H, Fang X, Zhang Y, Jin C (2018) Auxin acts downstream of ethylene and nitric oxide to regulate magnesium deficiency-induced root hair development in Arabidopsis thaliana. Plant Cell Physiol 59(7):1452–1465. https://doi.org/10.1093/pcp/pcy078
Maestre, R. B., M. Perez, J. Mendez-Natera and J. Farinas (2012). Effect of calcium fertilization on the production, distribution and quality of seeds of Arachis pintoi. Revista De La Facultad De Agronomia De La Universidad Del Zulia 29(1): 104–123. doi, <Go to ISI>://WOS:000303278600006
Mahmoud LM, Grosser JW, Dutt M (2020) Silver compounds regulate leaf drop and improve in vitro regeneration from mature tissues of Australian finger lime (Citrus australasica). Plant Cell, Tissue Organ Cult 141(3):455–464. https://doi.org/10.1007/s11240-020-01803-8
Marschner H, Romheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9(3):695–713. https://doi.org/10.1080/01904168609363475
Mohiuddin A, Chowdhury M, Abdullah ZC, Napis S (1997) Influence of silver nitrate (ethylene inhibitor) on cucumber in vitro shoot regeneration. Plant Cell Tissue & Organ Cult 51(1):75–78. https://doi.org/10.1023/A:1005814514409
Morrissey J, Guerinot ML (2009) Iron uptake and transport in plants: the good, the bad, and the ionome. Chem Rev 109(10):4553–4567. https://doi.org/10.1021/cr900112r
Pons S, Fournier S, Chervin C, Becard G, Rochange S, Frey NFD et al (2020) Phytohormone production by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Plos One 15(10):e0240886. https://doi.org/10.1371/journal.pone.0240886
Puig S, Andres-Colas N, Garcia-Molina A, Penarrubia L (2007) Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant Cell Environ 30(3):271–290. https://doi.org/10.1111/j.1365-3040.2007.01642.x
Rahman A, Amakawa T, Goto N, Tsurumi S (2001) Auxin is a positive regulator for ethylene-mediated response in the growth of arabidopsis roots. Plant Cell Physiol 42(3):301–307. https://doi.org/10.1093/pcp/pce035
Romera FJ, Alcantara E (1994) Iron-deficiency stress responses in cucumber (Cucumis sativus L.) roots (a possible role for ethylene?). Plant Physiol 105(4):1133–1138. https://doi.org/10.1104/pp.105.4.1133
Romera FJ, Alcantara E (2004) Ethylene involvement in the regulation of Fe-deficiency stress responses by strategy I plants. Funct Plant Biol 31(4):315–328. https://doi.org/10.1071/FP03165
Romera FJ, García MJ, Alcántara E, Pérez-Vicente R (2011) Latest findings about the interplay of auxin, ethylene and nitric oxide in the regulation of Fe deficiency responses by strategy I plants. Plant Signal Behav 6(1):167–170. https://doi.org/10.4161/psb.6.1.14111
Schmidt W, Tittel J, Schikora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiol 122(4):1109–1118. https://doi.org/10.1104/pp.122.4.1109
Shi GR, Su GQ, Lu ZW, Liu CF, Wang XM (2014) Relationship between biomass, seed components and seed Cd concentration in various peanut (Arachis hypogaea L.) cultivars grown on Cd-contaminated soils. Ecotoxicol Environ Saf 110:174–181. https://doi.org/10.1016/j.ecoenv.2014.09.003
Singh N, Bhatla SC (2018) Nitric oxide regulates lateral root formation through modulation of ACC oxidase activity in sunflower seedlings under salt stress. Plant Signal Behav 13(5):e1473683. https://doi.org/10.1080/15592324
Stephens AM, Dean LL, Davis JP, Osborne JA, Sanders TH (2010) Peanuts, Peanut oil, and fat free peanut flour reduced cardiovascular disease risk factors and the development of atherosclerosis in Syrian golden hamsters. J Food Sci 75(4):H116–H122. https://doi.org/10.1111/j.1750-3841.2010.01569.x
Su CL, Zhang FM, Sun K, Zhang W, Dai CC (2019) Fungal endophyte phomopsis liquidambari improves iron and molybdenum nutrition uptake of peanut in consecutive monoculture soil. J Soil Sci Plant Nutr 19(1):71–80. https://doi.org/10.1007/s42729-019-0011-2
Sun HW, Feng F, Liu J, Zhao QZ (2017) The interaction between auxin and nitric oxide regulates root growth in response to iron deficiency in rice. Front Plant Sci. https://doi.org/10.3389/fpls.2017.02169
Tang MJ, Lu F, Yang Y, Sun K, Zhu Q, Xu FJ et al (2021) Benefits of endophytic fungus Phomopsis liquidambaris inoculation for improving mineral nutrition, quality, and yield of rice grains under low nitrogen and phosphorus condition. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10462-8
Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF et al (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14(6):1223–1233. https://doi.org/10.1105/tpc.001388
Viollier E, Inglett PW, Hunter K, Roychoudhury AN, Van Cappellen P (2000) The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl Geochem 15(6):785–790. https://doi.org/10.1016/S0883-2927(99)00097-9
Wang Y, Zhang WZ, Liu WK, Ahammed GJ, Wen WX, Guo SR et al (2021) Auxin is involved in arbuscular mycorrhizal fungi-promoted tomato growth and NADP-malic enzymes expression in continuous cropping substrates. BMC Plant Biol 21(1):48. https://doi.org/10.1186/s12870-020-02817-2
Waters BM, Blevins DG (2000) Ethylene production, cluster root formation, and localization of iron(III) reducing capacity in Fe deficient squash roots. Plant Soil 225(1–2):21–31. https://doi.org/10.1023/A:1026513022280
Wu JJ, Wang CA, Zheng LQ, Wang L, Chen YL, Whelan J et al (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(2):667–674. https://doi.org/10.1093/jxb/erq301
Xie XG, Fu WQ, Zhang FM, Shi XM, Zeng YT, Li H et al (2017) The endophytic fungus Phomopsis liquidambari increases nodulation and N-2 fixation in Arachis hypogaea by enhancing hydrogen peroxide and nitric oxide signalling. Microb Ecol 74(2):427–440. https://doi.org/10.1007/s00248-017-0944-8
Yang TJW, Perry PJ, Ciani S, Pandian S, Schmidt W (2008) Manganese deficiency alters the patterning and development of root hairs in Arabidopsis. J Exp Bot 59(12):3453–3464. https://doi.org/10.1093/jxb/ern195
Yang B, Wang XM, Ma HY, Jia Y, Li X, Dai CC (2014) Effects of the fungal endophyte Phomopsis liquidambari on nitrogen uptake and metabolism in rice. Plant Growth Regul 73(2):165–179. https://doi.org/10.1007/s10725-013-9878-4
Zhang W, Sun K, Shi RH, Yuan J, Wang XJ, Dai CC (2018) Auxin signalling of Arachis hypogaea activated by colonization of mutualistic fungus Phomopsis liquidambari enhances nodulation and N-2-fixation. Plant, Cell Environ 41(9):2093–2108. https://doi.org/10.1111/pce.13170
Zhu XF, Zhu CQ, Zhao XS, Zheng SJ, Shen RF (2016) Ethylene is involved in root phosphorus remobilization in rice (Oryza sativa) by regulating cell-wall pectin and enhancing phosphate translocation to shoots. Ann Bot 118(4):645–653. https://doi.org/10.1093/aob/mcw044
Acknowledgements
We acknowledge the National Natural Science Foundation of China (Grant No. 31870478), Program for Jiangsu Excellent Scientific and Technological Innovation team (17CXTD00014), and a project funded by the Priority Academic Program Development (PAPD) of the Jiangsu Higher Education Institutions of China.
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All authors contributed to the study conception and design. Material preparation and data collection were performed by Y-CD, L-JK, C-YM, and C-CD; data analysis was performed by WZ and KS. The first draft of the manuscript was written by Y-CD and C-CD, all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Supplementary file1 (JPG 76 kb) Effect of P. liquidambaris on the lateral root of peanut (a) Effect of P. liquidambaris on the peanuts lateral root appearance under different Fe states. (b) Effect of P. liquidambaris on the development of peanut root under different Fe states (c) Effect of P. liquidambaris on the root hairs of peanuts under different Fe states (d) Effect of P. liquidambaris on the lateral root number under different Fe states. (The data shown are the mean ± SD, *p < 0.05, **p < 0.01.). E =P. liquidambaris inoculation. -Fe = 2 μmol FeEDTA in Hogland nutrition. CK = 100 μmol FeEDTA in Hogland nutrition
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Supplementary file3 (JPG 603 kb) Effects of different concentrations of ACC and STS on the root ethylene, fresh weight and chlorophyll content of peanuts under Fe deficiency (2 μmol Fe in Hogland nutrition) (a) Effect of different concentrations of ACC and STS on the ethylene production of peanuts under Fe deficiency. (The data shown are the mean ± SD. Different letters indicate significant differences between treatments). (b) Effect of different concentrations of ACC on the fresh weight and chlorophyll of peanut under Fe deficiency. (The data shown are the mean ± SD, *p < 0.05, **p < 0.01). (c) Effect of different concentrations of STS on the fresh weight and chlorophyll of peanut under Fe deficiency. (The data shown are the mean ± SD, *p < 0.05, **p < 0.01). (d) Effect of different concentrations of ACC and STS on the Fe concentration of peanut under Fe deficiency. (The data shown are the mean ± SD. Different letters indicate significant differences between treatments)
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Supplementary file4 (JPG 3655 kb) Effects of different concentrations of IAA, L-Kyn and PCIB on the root IAA content, fresh weight, and chlorophyll of peanuts under Fe deficiency (2 μmol Fe in Hogland nutrition) (a) Effect of different concentrations of IAA, L-Kyn, and PCIB on the IAA content of peanuts (The data shown are the mean ± SD. Different letters indicate significant differences between treatments). (b) Effect of different concentrations of IAA on the fresh weight and chlorophyll of peanuts. (The data shown are the mean ± SD, *p < 0.05, **p < 0.01.). (c) Effect of different concentrations of L-Kyn on the fresh weight and chlorophyll of peanuts. (The data shown are the mean ± SD, *p < 0.05, **p < 0.01). (d) Effect of different concentrations of PCIB on the fresh weight and chlorophyll of peanuts. (The data shown are the mean ± SD, *p < 0.05, **p < 0.01). (e) Effect of different concentrations of IAA, L-Kyn, and PCIB on Fe concentration of peanuts. (The data shown are the mean ± SD. Different letters indicate significant differences between treatments)
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Supplementary file6 (JPG 216 kb) Effect of P. liquidambaris on pH in different treatment groups The peanuts were transferred to the Hoagland nutrient solution. pH was detected with a digital pH meter. (The data shown are the mean ± SD.). E =P. liquidambaris inoculation. -Fe = 2 μmol FeEDTA in Hogland nutrition. CK = 100 μmol FeEDTA in Hogland nutrition
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Supplementary file7 (DOCX 13 kb) Colonization of P. liquidambaris in different treatment groups The peanuts were transferred to the Hoagland nutrient solution. Seven days after the addition of P. liquidambaris, the colonization was detected by q-PCR. (The data shown are the mean ± SD.). E =P. liquidambaris inoculation. -Fe = 2 μmol FeEDTA in Hogland nutrition. CK = 100 μmol FeEDTA in Hogland nutrition
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Du, YC., Kong, LJ., Ma, CY. et al. Auxin Functions Downstream of Ethylene to Regulate Iron Absorption Promoted by Phomopsis liquidambaris in Arachis hypogaea L.. J Plant Growth Regul 42, 1879–1892 (2023). https://doi.org/10.1007/s00344-022-10666-6
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DOI: https://doi.org/10.1007/s00344-022-10666-6