Abstract
Dynamic changes in growth characteristics and endogenous hormone contents in the leaves and roots of Sophora davidii seedlings under low-phosphorus stress were studied to provide a reference for further study of the internal regulatory mechanism of the response strategy of this species to low-phosphorus stress. Normal phosphorus (0.5 mmol KH2PO4, NP) and low-phosphorus (0.005 mmol KH2PO4, LP) levels and different treatment times were applied to study growth characteristics, phosphorus utilization and hormone contents in the leaves and roots of potted Sophora davidii by tissue culture and sand culture. The results first showed that compared with NP, LP significantly decreased the plant height, leaf length, leaf width, leaf area, leaf perimeter and root–shoot ratio by 20.10%, 21.08%, 22.73%, 51.33%, 24.94% and 18.92%, respectively. LP decreased the total root length and root dry weight, and increased the root surface area, average root diameter, root tip number, root volume and dry weight of the aerial part on day 9, but these effects were not significant. Second, compared with NP, LP significantly decreased P contents in the aerial part and roots and P uptake efficiency in the aerial part and roots on day 9 by 23.33%, 53.89%, 14.04% and 58.06%, respectively. LP significantly increased the P utilization efficiency and leaf acid phosphatase (ACP) activity on day 9 by 82.79% and 84.38%, respectively. LP increased root ACP activity on day 9, but the effect was not significant. Third, compared with NP, LP significantly decreased abscisic acid (ABA), cytokinin (CTK) and strigolactone (SL) contents in leaves by 21.52%, 36.65% and 45.86%, respectively, and significantly increased gibberellin (GA) contents in roots by 28.92% on day 9. LP decreased GA contents in leaves and CTK contents in roots and increased indole-3-acetic acid (IAA) contents in leaves and roots and ABA and SL contents in roots on day 9, but these effects were not significant. Correlation analysis indicated that endogenous hormone contents in Sophora davidii leaves and roots under different treatment conditions had certain correlations with growth characteristics. In conclusion, Sophora davidii can improve its P utilization efficiency by changing growth characteristics and endogenous hormones to enhance its adaptive response to low-phosphorus stress.
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References
Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. In: Merchant SS (ed.) Ann Rev Plant Biol 66(1): 161–186. https://doi.org/10.1146/annurev-arplant-043014-114759.
Bayuelo-Jimenez JS, Ochoa I, Perez-Decelis VA, de Loudes M-A, Cardenas-Navarro R (2012) Phosphorus-efficiency in maize germplasm at seedling stage from the P’urhepecha plateau. Rev Fitotec Mex 35(3):199–208
Bray EA (2010) Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environm 25(2):153–161. https://doi.org/10.1046/j.1365-3040.2002.00746.x
Cao P, Ren Y, Zhang K, Teng W, Zhao X, Dong Z, Liu X, Qin H, Li Z, Wang D, Tong Y (2014) Further genetic analysis of a major quantitative trait locus controlling root length and related traits in common wheat. Mol Breed 33(4):975–985. https://doi.org/10.1007/s11032-013-0013-z
Chapman HD, Pratt PF (1962) Methods of analysis for soils, plants and waters. Soil Sci 93(1):68
Czarnecki O, Yang J, Weston DJ, Tuskan GA, Chen J (2013) A dual role of strigolactones in phosphate acquisition and utilization in plants. Int J Mol Sci 14(4):7681–7701. https://doi.org/10.3390/ijms14047681
Deng Y, Men C, Qiao S, Wang W, Yang J (2020) Tolerance to low phosphorus in rice varieties is conferred by regulation of root growth. Crop J 8(4): 534–547. https://doi.org/10.1016/j.cj.2020.01.002
Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG (2009) Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant 2(1):43–58. https://doi.org/10.1093/mp/ssn081
Du Y, Scheres B (2018) Lateral root formation and the multiple roles of auxin. J Experim Botany 69:155–167. https://doi.org/10.1093/jxb/erx223
Gho Y, An G, Park H, Jung K (2018) A systemic view of phosphate starvation-responsive genes in rice roots to enhance phosphate use efficiency in rice. Plant Biotechnol Rep 12(4):249–264. https://doi.org/10.1007/s11816-018-0490-y
Giehl RFH, Gruber BD, von Wiren N (2014) Its time to make changes: modulation of root system architecture by nutrient signals. J Experim Botany 65(3):769–778. https://doi.org/10.1093/jxb/ert421
Harvey PR, Warren RA, Wakelin S (2009) Potential to improve root access to phosphorus: the role of non-symbiotic microbial inoculants in the rhizosphere. Crop Pasture Ence 60(2):144–151. https://doi.org/10.1071/CP08084
Jia H, Zhang S, Wang L, Yang Y, Zhang H, Cui H, Shao H, Xu G (2017a) OsPht1;8, a phosphate transporter, is involved in auxin and phosphate starvation response in rice. J Experim Botany 68(18):5057–5068. https://doi.org/10.1093/jxb/erx317
Jia Z, Zhang Q, Tong Z, Li Y, Xu H, Wang X, Bi S, Cao J, He F, Wang L, Li X (2017b) Analysis of morphological and physiological responses to low Pi stress in different alfalfas. Scientia Agricultura Sinica 50(20):3898–3907. https://doi.org/10.3864/j.issn.0578-1752.2017.20.006
Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145(4):1460–1470. https://doi.org/10.1104/pp.107.103788
Johnston AE, Poulton PR, Fixen PE, Curtin D (2014) Phosphorus: its efficient use in agriculture. Adv Agron 123:177–228. https://doi.org/10.1016/B978-0-12-420225-2.00005-4
Kapulnik Y, Koltai H (2016) Fine-tuning by strigolactones of root response to low phosphate. J Intege Plant Biol 58:203–212. https://doi.org/10.1111/jipb.12454
Kisko M, Bouain N, Rouached A, Choudhary SP, Rouached H (2015) Molecular mechanisms of phosphate and zinc signalling crosstalk in plants: Phosphate and zinc loading into root xylem in Arabidopsis. Environm Experim Botany 114:57–64. https://doi.org/10.1016/j.envexpbot.2014.05.013
Lin B, Liu X, Wu S, Zheng H, Huo K, Qi S, Chen C (2019) phytochemicals content, antioxidant and antibacterial activities of Sophora viciifolia. Chem Biodiv 16(7). https://doi.org/10.1002/cbdv.201900080
Liu Q, Zhou GQ, Xu F, Yan XL, Liao H, Wang JX (2013) The involvement of auxin in root architecture plasticity in Arabidopsis induced by heterogeneous phosphorus availability. Biol Plant 57(4):739–748. https://doi.org/10.1007/s10535-013-0327-z
Liu Y, Li X, Wang R, Zhang C (2015) Screen indexes for soybean tolerance to phosphorus deficiency and identification of low-P tolerant soybean varieties. J Agric Sci Technol 17: 30–41. https://doi.org/10.13304/j.nykjdb.2015.349. (Chinese)
Liu G, Pfeifer J, Francisco RDB, Emonet A, Stirnemann M, Gubeli C, Hutter O, Sasse J, Mattheyer C, Stelzer E, Walter A, Martinoia E, Borghi L (2018) Changes in the allocation of endogenous strigolactone improve plant biomass production on phosphate-poor soils. New Phytol 217(2):784–798. https://doi.org/10.1111/nph.14847
Marquez-Lopez RE, Quintana-Escobar AO, Loyola-Vargas VM (2019) Cytokinins, the Cinderella of plant growth regulators. Phytochem Rev 18:1387–1408. https://doi.org/10.1007/s11101-019-09656-6
Meng ZB, You XD, Suo D, Chen YL, Tang C, Yang JL, Zheng SJ (2013) Root-derived auxin contributes to the phosphorus-deficiency-induced cluster-root formation in white lupin (Lupinus albus). Physiol Plant 148(4):481–489. https://doi.org/10.1111/j.1399-3054.2012.01715.x
Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155(2):1000–1012. https://doi.org/10.1104/pp.110.165191
Mueller M, Munne-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods. https://doi.org/10.1186/1746-4811-7-37
Nadira UA, Ahmed IM, Wu F, Zhang G (2016) The regulation of root growth in response to phosphorus deficiency mediated by phytohormones in a Tibetan wild barley accession. Acta Physiol Plant. https://doi.org/10.1007/s11738-016-2124-8
Normanly J (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harbor Perspect Biol. https://doi.org/10.1101/cshperspect.a001594
Pang J, Yang J, Lambers H, Tibbett M, Siddique KHM, Ryan MH (2015) Physiological and morphological adaptations of herbaceous perennial legumes allow differential access to sources of varyingly soluble phosphate. Physiol Plant 154(4):511–525. https://doi.org/10.1111/ppl.12297
Postma JA, Lynch JP (2011) Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Annal Botany 107:829–841. https://doi.org/10.1093/aob/mcq199
Radin JW, Parker LL, Guinn G (1982) Water Relations of cotton plants under nitrogen deficiency: V. environmental control of abscisic acid accumulation and stomatal sensitivity to abscisic acid. Plant Physiol 70(4):1066–1070. https://doi.org/10.1104/pp.70.4.1066
Ren P (2018) Evaluation of Phosphorus Use Efficiency and Transcriptome Analysis in Barley Germplasm (Hordeum vulgare L.). Gansu Agricultural University, 125 (Chinese)
Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156. https://doi.org/10.1007/s11104-011-0950-4
Schaefer M, Bruetting C, Meza-Canales ID, Grosskinsky DK, Vankova R, Baldwin IT, Meldau S (2015) The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions. J Experim Botany 66:4873–4884. https://doi.org/10.1093/jxb/erv214
Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53(366):33–37. https://doi.org/10.1093/jexbot/53.366.33
Shen Y, Zhang Y, Lin H, Gao S, Pan G (2012) Effect of low phosphorus stress on endogenous hormone levels of different maize genotypes in seedling stage. J Biolog Sci. https://doi.org/10.3923/jbs.2012.308.314
Shen J, Li C, Mi G, Li L, Yuan L, Jiang R, Zhang F (2013) Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. J Experim Botany 64(5):1181–1192. https://doi.org/10.1093/jxb/ers342
Shi T, Zhao D, Li D, Wang N, Meng J, Xu F, Shi L (2012) Brassica napus root mutants insensitive to exogenous cytokinin show phosphorus efficiency. Plant Soil 358(1–2):57–70. https://doi.org/10.1007/s11104-012-1219-2
Strock CF, de la Riva LM, Lynch JP (2018) Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition. Plant Physiol 176(1):691–703. https://doi.org/10.1104/pp.17.01583
Sun H, Bi Y, Tao J, Huang S, Hou M, Xue R, Liang Z, Gu P, Yoneyama K, Xie X, Shen Q, Xu G, Zhang Y (2016) Strigolactones are required for nitric oxide to induce root elongation in response to nitrogen and phosphate deficiencies in rice. Plant Cell Environm 39(7):1473–1484. https://doi.org/10.1111/pce.12709
Sun L, Wang L, Zheng Z, Liu D (2018) Identification and characterization of an Arabidopsis phosphate starvation-induced secreted acid phosphatase as a vegetative storage protein. Plant Sci 277:278–284. https://doi.org/10.1016/j.plantsci.2018.09.016
Tang H, Shen J, Zhang F, Rengel Z (2013) Interactive effects of phosphorus deficiency and exogenous auxin on root morphological and physiological traits in white lupin (Lupinus albus L). Sci China-Life Sci 56(4):313–323. https://doi.org/10.1007/s11427-013-4461-9
Tang H, Chen X, Gao Y, Hong L, Chen Y (2020) Alteration in root morphological and physiological traits of two maize cultivars in response to phosphorus deficiency. Rhizosphere. https://doi.org/10.1016/j.rhisph.2020.100201
Tyburski J, Dunajska K, Tretyn A (2010) A role for redox factors in shaping root architecture under phosphorus deficiency. Plant Signal Behav 5(1):64–66
van de Wiel CCM, van der Linden CG, Scholten OE (2016) Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207(1):1–22. https://doi.org/10.1007/s10681-015-1572-3
Van Lam N, Stangoulis J (2019) Variation in root system architecture and morphology of two wheat genotypes is a predictor of their tolerance to phosphorus deficiency. Acta Physiol Plant. https://doi.org/10.1007/s11738-019-2891-0
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecolog Applic 20(1):5–15. https://doi.org/10.1890/08-0127.1
Vysotskaya LB, Trekozova AW, Kudoyarova GR (2016) Effect of phosphorus starvation on hormone content and growth of barley plants. Acta Physiol Plant. https://doi.org/10.1007/s11738-016-2127-5
Waadt R, Hsu P, Schroeder JI (2015) Abscisic acid and other plant hormones: Methods to visualize distribution and signaling. BioEssays 37(12):1338–1349. https://doi.org/10.1002/bies.201500115
Wang Z, Rahman ABMM, Wang G, Ludewig U, Shen J, Neumann G (2015) Hormonal interactions during cluster-root development in phosphate-deficient white lupin (Lupinus albus L.). J Plant Physiol 177:74–82. https://doi.org/10.1016/j.jplph.2014.10.022
Wang H, Wang P, Zhao G, Sun Q, Long Z, Zhang Y (2016) Seed size and germination strategy of Sophora davidii under drought stress. Acta Ecol Sin 36:335–341. https://doi.org/10.5846/stxb201312032878
Wang YZ, Chen X, Lu CY, Huang B, Shi Y (2018a) Different mechanisms of organic and inorganic phosphorus release from Mollisols induced by low molecular weight organic acids. Canadian J Soil Sci. https://doi.org/10.1139/cjss-2017-0002
Wang L, Zhu J, Xiaoming S (2018b) Salt and drought stress and ABA responses related to bZIP genes from V. radiata and V. angularis. Gene Int J Focus Gene Clon Gene Str Funct 651:152–160. https://doi.org/10.1016/j.gene.2018.02.005
Wang Y, Li L, Wang R, Tang L, Zheng Y (2020) Change of root morphology in intercropping systems of wheat and faba bean under different phosphorus levels and its relationship with endogenous hormones. Chinese J Appl Ecol. https://doi.org/10.13287/j.1001-9332.202009.029 (Chinese)
Wu L, Wei X, Lu W, Li T, Yao Q, Zhao X (2018) Effects of seed vigor at different harvesting time and drought-heat stress on growth and development of Sophora davidii seedlings. Jiangsu Agric Sci 46(16):94–98. https://doi.org/10.15889/j.issn.1002-1302.2018.16.023 (Chinese)
Xiong R, Tang H, Xu M, Zeng C, Peng Y, He R, Yan Z, Qi Z, Cheng Y (2018) Transcriptomic analysis of banana in response to phosphorus starvation stress. AGRONOMY-BASEL. https://doi.org/10.3390/agronomy8080141
Yamagishi M, Zhou K, Osaki M, Miller SS, Vance CP (2011) Real-time RT-PCR profiling of transcription factors including 34 MYBs and signaling components in white lupin reveals their P status dependent and organ-specific expression. Plant Soil 342(1–2):481–493. https://doi.org/10.1007/s11104-010-0711-9
Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T (2007) Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol 143(3):1362–1371. https://doi.org/10.1104/pp.106.091561
Yu J, Li Y, Yin D, Zhou C, Ma X (2017) Response and physiological mechanism of Chinese fir to low phosphorus stress. Forest Res 30: 566–575. https://doi.org/10.13275/j.cnki.lykxyj.2017.04.005 (Chinese)
Zhang J, Jiang F, Shen Y, Zhan Q, Bai B, Chen W, Chi Y (2019a) Transcriptome analysis reveals candidate genes related to phosphorus starvation tolerance in sorghum. BMC Plant Biol. https://doi.org/10.1186/s12870-019-1914-8
Zhang S, Tang D, Helena K, Li C (2019b) Metabolic and physiological analyses reveal that Populus cathayana males adopt an energy saving strategy to cope with phosphorus deficiency. Tree Physiol 39(9):1630–1645. https://doi.org/10.1093/treephys/tpz074
Zou X, Wu P, Chen N, Wang P, Ma X (2015) Chinese fir root response to spatial and temporal heterogeneity of phosphorus availability in the soil. Canadian J Forest Res 45(4):402–410. https://doi.org/10.1139/cjfr-2014-0384
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This work was funded through projects of the National Key Research and Development Programme of China (2016YFC0502607-04), the National Natural Science Foundation of China (31702173), and Science and Technology Project of Guizhou Province (QKHZC[2019]2295).
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Zhao, X., Zhao, LL., Huang, LJ. et al. Response of growth characteristics and endogenous hormones of Sophora davidii to low-phosphorus stress. Acta Physiol Plant 43, 118 (2021). https://doi.org/10.1007/s11738-021-03284-4
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DOI: https://doi.org/10.1007/s11738-021-03284-4