Abstract—
Knowledge of the composition and volume of root-exuded organic substances is crucial for understanding the biochemical processes in the rhizosphere. The present study was undertaken to quantify organic acids from the roots of drought-tolerant and non-drought-tolerant rice cultivars (DTR and NDTR) and their response to irrigation during different growth periods. Alternating wetting and moderate drying with 4 cm water layer of flood irrigation until the soil water potential reaches −15 kilopascal (kPa) (WMD) significantly enhanced succinic, maleic, citric, malic, oxalic, tartaric, and total organic acids in the two rice cultivars during the trial by 80.59–86.68, 31.62–58.55, 16.55–43.00, 17.89–25.66, 13.68–29.70, 12.40–16.05, and 17.34–21.24%, respectively. Alternate wetting and severe drying with 4 cm water layer of irrigation until the soil water potential reached −30 kPa (WSD) notably decreased formation of maleic, citric, malic, oxalic, tartaric, and total organic acids in the two rice cultivars during the experiment by 5.19–25.15, 13.96–29.92, 20.81–34.88, 32.20–42.51, 12.79–24.66, and 6.67–24.22%, respectively. Acetic acid output between CF (continuous flooding with a 3–4 cm water layer) and WMD treatments in pads with two rice cultivars did not differ. The WSD treatment increased acetic acid exudation by 16.93–25.99% in two rice cultivars during the experiment. The high content of acetic and total organic acids in DTR should be responsible for the smaller loss of total organic acids in the WSD treatment and the high drought tolerance capacity. The results contribute to valuable background knowledge for exploring the role of root exudates in soil-plant relationships.
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INTRODUCTION
Crops, such as corn and wheat, and particularly irrigated rice (Oryza sativa L.), consume large quantities of water [27, 34], which is the lifeline of crop productivity worldwide. In the context of increasing competition between agriculture, industry, and urban populations for finite water resources, different water management practices for a high water-use efficiency were explored in the agricultural sector. Current studies have shown that water management practices synchronously affect plant growth [12], grain yield [5, 26], and grain quality [6, 9], which are closely associated with root morphology and physiology [42]. Plant roots not only are critical vegetative organs that absorb and transport water and nutrients throughout the life span of plants [29], but also release ions and large amounts of organic substances into the soil, namely root exudates [10, 13]. However, previous studies about the effects of water management practices have focused on root morphology (e.g., root length, distribution, depth, and density) [20–22, 32, 38, 45], the effects on root exudates has received comparatively little attention.
Root exudates play a crucial role in below-ground interactions between plants, soil, and microorganisms [4], including the facilitation of the absorption of nutrients by plants [11], regulating plant responses to environmental stress [18, 40], forming the rhizosphere microbial community [15, 36], and stimulating soil nitrogen transformations [25, 44]. Among various root exudates, organic acids (e.g., acetic, citric, or succinic acid) are essential components of various processes operating in the rhizosphere, including nutrient acquisition [1, 23, 47], alleviation of root environmental stress, pathogen attraction, mineral weathering [19], and metal detoxification [17, 43], which should positively contribute to plant growth and crop yield. Therefore, it is imperative to understand the response of root exudates including organic acids to environmental changes.
While various environmental conditions affect root-exuded organic acids, the majority of previous studies has concentrated on the effects of metal stresses (e.g., Cd [18], Tl [43], and Al [17, 30, 37]) and nutrition stresses (e.g., P deficiency [47], Mn excess [35], and Zn deficiency [46]). More recently, studies have investigated the influence of stresses originating from arsenic (As) [40], phenanthrene [28], biochar and nitrogen fertilizer exposure [41], and warming [8, 44] on root-exuded organic acids. However, the impact of water management on root-exuded organic acids remains poorly understood.
Irrigated rice contributes 75% of the world’s rice production [33] and has also the largest water consumption in the agricultural sector [34]. In the present study, we aimed to identify the response of organic acids in drought and non-drought tolerant rice root exudates to water management practices during different growth periods.
MATERIALS AND METHODS
Study site. Field experiments were conducted in Songyuan City (123°091′–124°221′ E, 44°571′–45°461′ N) of Western Jilin Province, Northeast China during the rice growth period (May–September) in 2018. The two rice cultivars (Jijing 113, non-drought tolerant rice, NDTR; Changbai 9, drought tolerant rice, DTR) have the same growth period. The paddy soil used with a pH of 7.4 contained 27.62 g kg−1 total organic carbon, 2.30 g kg−1 total N, 163.31 mg kg−1 available N, 42.75 mg kg−1 available P, and a bulk density of 1.32 g cm−3 in the 0–15 cm layer. The soil is classified as Anthrosols according to World Reference Base of Soil Resources (WRB).
Crop management practices. Rice seeds were sown in the greenhouse for nursery raising, and seedlings were transplanted manually to the field with a spacing of 30.0 × 16.6 cm. Irrigation water for all the treatments was taken from the groundwater. Plants in one row on each side of all the treatments were not considered for sampling to avoid border effects.
The same fertilization rates and timing were applied for all the treatments based on the local farming practice. 60 kg N ha−1 (urea), 90 kg P2O5 ha−1 (superphosphate), and 45 kg K2O ha−1 (potassium chloride) were applied and incorporated into the soil with a plough before transplanting. 60 kg N ha−1 was applied during the tillering period. 30 kg N ha−1 and 30 kg K2O ha−1 were applied during the heading period.
Experimental design. The experiment consisted of three treatments: (1) continuous flooding with a 3 to 4 cm water layer overlying the soil surface (CF); (2) alternate wetting and moderate drying with a 4 cm water layer of irrigation until the soil water potential reached −15 kilopascal (kPa) at a depth of 20 cm (WMD) and; (3) alternate wetting and severe drying with a 4 cm water layer of irrigation until the soil water potential reached −30 kPa at a depth of 20 cm (WSD). Each treatment was replicated three times. The nine plots were arranged in a randomized complete block design. Each plot was separated from adjacent plots by 3-m wide isolation strips. Each plot measured 4 m2 (2 × 2 m) and was bounded (10 cm height). A rain shelter comprising a steel-frame covered with plastic sheeting for each plot was used to minimize the influence of rainfall on the treatments, and the plastic sheeting was moved away after the rain.
Collection and measurement of organic acids. Five rice plants in each plot of each treatment were randomly selected in the mid-tillering and heading periods, respectively. The roots of the selected rice plants were cleaned using distilled water, after which they were dipped into 0.2 mmol L−1 CaCl2 solution and 20 mg L−1 chloramphenicol solution for 0.5 h, respectively. After cleaning with deionized water, the rice plants were transferred to beakers, which were covered by tinfoil. An equivalent deionized water was added to each beaker to flood the roots. The solutions in the beakers were collected after 4 h of incubation under sunshine and were concentrated to 5 mL using a vacuum rotatory evaporator (Yarong Re-52AA, Shanghai, China) for the determination of organic acids. The roots were collected, dried at 105°C, and weighed.
The contents of oxalic, acetic, citric, tartaric, malic, succinic, and maleic acids were determined after high performance liquid chromatography (HPLC) separation of the root exudates solution through a Bio-Rad Aminex HPX-87H chromatogram column with a HPLC (Waters 600, Waters Corporation, USA) equipped with an ultraviolet absorption detector (Waters 2996, Waters Corporation, USA). Chromatographic separation was performed under the following conditions: column temperature 50°C, mobile phase 5 mmol L−1 H2SO4 solution, flow rate of 0.5 mL min−1, and sample volume of 10 μL. The test wavelength was set to 210 nm. The values of detection limit of these organic acids range from 0.004 to 0.193 μg g−1. The organic acid contents were expressed as μg g−1 of dry root weight (μg g−1 DW). Total contents of organic acids were calculated as the sum of the abovementioned organic acids.
Statistical analysis. Statistical analysis of the experimental data was performed using the SPSS 25.0 software (International Business Machines Corporation, New York, America). All figures were drawn using Sigmaplot 14.0 (Systat Software, Inc., San Jose, CA, USA).
RESULTS
The concentrations of succinic, acetic, maleic, and citric acids in NDTR in the CF treatment were 102.45, 168.74, 12.68, and 125.36 μg g−1 DW during the mid-tillering period and significantly increased by 54.95, 41.36, 40.77, and 49.69% during the heading period, respectively (Fig. 1). Compared to the concentration of succinic (121.76 μg g−1 DW), acetic (693.41 μg g−1 DW), maleic (13.69 μg g−1 DW), and citric acid (133.62 μg g−1 DW) in DTR in the CF treatment during the mid-tillering period, those during the heading period were increased by 17.66, 18.38, 19.14, and 73.23%, respectively. The roots of DTR in the CF treatment during the mid-tillering period released markedly more succinic (by 18.85%) and acetic acids (by 310.91%) than those of NDTR. The roots of NDTR in the CF treatment during the heading period exuded notably more succinic (by 10.81%) and maleic acids (by 9.44%), but less acetic (by 70.94%) and citric acids (by 18.93%) than those of DTR.
Compared to the concentrations of maleic and citric acids in the CF treatment of the two rice cultivars in the two periods, those in the WMD treatment significantly increased by 31.62–58.55 and 16.55–43.00%, while those in the WSD treatment notably declined by 5.19–25.15 and 13.96–29.92%, respectively (Fig. 1). The WMD treatment did not influence the concentration of acetic acid. The WSD treatment enhanced the concentration of acetic acid by 16.93–25.99% in the two rice cultivars in the two periods compared to the CF treatment. The roots of the two rice cultivars in the WMD treatment exuded 80.59–86.68% higher concentrations of succinic acid than those in the CF treatment. Generally, the concentrations of succinic acid of the two cultivars did not differ between the CF and WSD treatments.
The concentrations of malic, oxalic, and tartaric acids of NDTR in the CF treatment during the heading period reached 576.42, 585.68, and 707.62 μg g−1 DW, which were 17.74, 17.99, and 12.62% higher than those during the mid-tillering period, respectively (Fig. 2). The concentrations of oxalic and tartaric acids of DTR in the CF treatment increased by 119.92 and 268.51 μg g−1 DW, respectively, from the mid-tillering to the heading period. Compared to the concentrations of malic, oxalic, and tartaric acids in the two cultivars in the CF treatment during the trial, those in the WMD treatment increased by 17.89–25.66, 13.68–29.70, and 12.40–16.05%, while those in the WSDM treatment declined by 20.81–34.88, 32.20–42.51, and 12.79–24.66%, respectively.
The concentration of total organic acids during the mid-tillering and heading periods in the CF treatment of NDTR were 2023.52 and 2472.51 μg g−1 DW, which were notably lower by 438.15 and 635.37 μg g−1 DW than those of DTR, respectively (Fig. 2). Compared to the concentration of total organic acids of NDTR and DTR in the CF treatment during the mid-tillering period, that of the two cultivars in the WMD treatment increased by 20.95 and 17.34%, that in the WSD treatment decreased by 21.92 and 6.67%, respectively. The concentration of total organic acids of NDTR and DTR in the CF treatment during the heading period was 16.75 and 17.52% lower than that in the WMD treatment, and was 31.97 and 14.03% higher than that in the WSDM treatment, respectively.
DISCUSSION
Root-exuded organic acids originate mainly from photosynthate [13]. The low release of organic acids observed during the mid-tillering period was likely due to the low photosynthetic capacity [31] and root biomass [3] of the rice at this growth stage, which inhibits the production and exudation of organic acids. This observation is supported by Aulakh et al., who observed the lowest release of root-exuded organic C and exudates in rice during the seedling period [3]. With rice plant growth, increases in photosynthesis and root biomass were observed, which led to increases in root exudates, including organic acids during the heading period. A study by Sakai et al. [31] reported a peak in the net photosynthetic rate of the rice canopy during the heading period with a concurrent exudation of a large amount of organic acids. Rice plants require large quantities of nutrients during the heading period, during which vegetative and reproductive growth occur simultaneously. This fact possibly explains the release of a large quantity of organic acids during the heading period as a vital mechanism to facilitate the release of soil nutrients and the subsequent absorption of these nutrients by the rice plants. Root-exuded oxalic, succinic, and citric acids promote the release of Mn [35] from the soil, whereas maleic and citric acids facilitate the release of Zn [23]. The increases in tartaric, malic, and succinic acids contribute to the mobilization of soluble P [47]. Other studies have found that malic and citric acids mobilize Fe and Mn by contact reduction, whereas citric, oxalic, tartaric, and malic acids mobilize P, Fe, Zn, and Mn by metal chelation [24]. In addition, the increases in root biomass and activity during the heading period [3] further facilitate the exudation of organic acids from roots.
Although both the WMD and WSD treatments could provide better soil aeration for root respiration than the CF treatment, the WMD treatment could sufficiently provide water for rice growth, while the WSD treatment could not. Therefore, the WMD treatment likely provides a more suitable environment for root metabolism and for the supply of nutrients and energy to the aboveground rice organs as compared to the CF treatment. The WSD treatment resulted in the severe damage of the physiological function of the roots and aboveground rice organs [16]. Moderate dying in the WMD treatment improved the root and shoot biomass and the root oxidation activity of rice compared to that in the CF treatment, while severe drying in the WSD treatment led to a serious decline in root and shoot biomass and root oxidation activity [48]. The WSD treatment resulted in substantial decreases in leaf photosynthetic CO2 exchange rates, concentrations of chlorophyll, and total soluble protein, and a consequent decline in the photosynthetic rate [39] and lowered root exudates. Therefore, the WMD and WSD treatments, in general, maintained the highest and lowest levels of citric, succinic, maleic, oxalic, tartaric, malic, and total organic acids during the mid-tillering and heading periods, which could create a positive and negative feedback loop for plant growth and the physiological function of root exudates, including organic acids, respectively. The increased exudation of acetic acid in the two rice cultivars in the WSD treatment during the mid-tillering and heading periods can be explained as a mechanism for enduring drought stress [2]. Previous studies showed that plant roots would increase the exudation of several root exudate fractions to reduce negative effects on plant growth [7, 14], indicating that increased root exudate fractions should be the key factor to endure drought stress. Therefore, the high root-exuded acetic acids of DTR should be responsible for its strong drought resistance and for the subsequent smaller loss in total organic acids in the WSD treatment. In addition, the high root-exuded total organic acids of DTR might lead to its high nutrient absorption and recovery capacities [14], and the subsequent high adaptability to drought. The differences of root-exuded organic acids between the two rice cultivars primarily resulted from their different genotypes and phenotypes [3].
CONCLUSIONS
WMD facilitated the production of root-exuded total organic acids of rice, but WSD inhibited the production of root-exuded total organic acids. The high concentrations of root-exuded organic acids, particularly acetic acid, of DTR should to some extent be responsible for its high drought tolerance.
REFERENCES
D. S. Almeida, D. Menezes-Blackburn, B. L. Turner, C. Wearing, P. M. Haygarth, and C. A. Rosolem “Urochloa ruziziensis cover crop increases the cycling of soil inositol phosphates,” Biol. Fert. Soils 54, 935–947 (2018). https://doi.org/10.1007/s00374-018-1316-3
M. Ashrafi, M. R. Azimi-Moqadam, P. Moradi, E. MohseniFard, F. Shekari, and M. Kompany-Zareh “Effect of drought stress on metabolite adjustments in drought tolerant and sensitive thyme,” Plant Physiol. Biochem. 132, 391–399 (2018). https://doi.org/10.1016/j.plaphy.2018.09.009
M. S. Aulakh, R. Wassmann, C. Bueno, J. Kreuzwieser, and H. Rennenberg “Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars,” Plant Biol. 3, 139–148 (2001). https://doi.org/10.1055/s-2001-12905
D. R. Batish, K. Lavanya, H. P. Singh, and R. K. Kohli “Root-mediated allelopathic interference of nettle-leaved goosefoot (Chenopodium murale) on wheat (Triticum aestivum),” J. Agron. Crop Sci. 193, 37–44 (2007). https://doi.org/10.1111/j.1439-037X.2006.00243.x
M. Ben Hassen, F. Monaco, A. Facchi, M. Romani, G. Vale, and G. Sali “Economic performance of traditional and modern rice varieties under different water management systems,” Sustainability 9, 347 (2017). https://doi.org/10.3390/su9030347
R. J. Bryant, M. Anders, and A. McClung “Impact of production practices on physicochemical properties of rice grain quality,” J. Sci. Food Agric. 92, 564–569 (2012). https://doi.org/10.1002/jsfa.4608
A. Cesari, N. Paulucci, M. Lopez-Gomez, J. Hidalgo-Castellanos, C. Lluch Pla, and M. Susana Dardanelli “Restrictive water condition modifies the root exudates composition during peanut-PGPR interaction and conditions early events, reversing the negative effects on plant growth,” Plant Physiol. Biochem. 142, 519–527 (2019). https://doi.org/10.1016/j.plaphy.2019.08.015
N. Cheng, Y. Peng, Y. Kong, J. Li, and C. Sun “Combined effects of biochar addition and nitrogen fertilizer reduction on the rhizosphere metabolomics of maize (Zea mays L.) seedlings,” Plant Soil 433, 19–35 (2018). https://doi.org/10.1007/s11104-018-3811-6
W. D. Cheng, G. P. Zhang, G. P. Zhao, H. G. Yao, and H. M. Xu “Variation in rice quality of different cultivars and grain positions as affected by water management,” Field Crops Res. 80, 245–252 (2003). https://doi.org/10.1016/s0378-4290(02)00193-4
G. Cieslinski, K. C. J. VanRees, A. M. Szmigielska, and P. M. Huang “Low molecular weight organic acids released from roots of durum wheat and flax into sterile nutrient solutions,” J. Plant Nutr. 20, 753–764 (1997). https://doi.org/10.1080/01904169709365291
F. D. Dakora and D. A. Phillips “Root exudates as mediators of mineral acquisition in low-nutrient environments,” Plant Soil 245, 35–47 (2002). https://doi.org/10.1023/a:1020809400075
A. Elazab, M. Dolors Serret, and J. Luis Araus “Interactive effect of water and nitrogen regimes on plant growth, root traits and water status of old and modern durum wheat genotypes,” Planta 244, 125–144 (2016). https://doi.org/10.1007/s00425-016-2500-z
Y. Gao, L. Ren, W. Ling, S. Gong, B. Sun, and Y. Zhang “Desorption of phenanthrene and pyrene in soils by root exudates,” Bioresour. Technol. 101, 115–1165 (2010). https://doi.org/10.1016/j.biortech.2009.09.062
A. Gargallo-Garriga, C. Preece, J. Sardans, M. Oravec, O. Urban, and J. Penuelas “Root exudate metabolomes change under drought and show limited capacity for recovery,” Sci. Rep. 8, 12696 (2018). https://doi.org/10.1038/s41598-018-30150-0
J. P. Guyonnet, M. Guillemet, A. Dubost, L. Simon, P. Ortet, M. Barrakat, T. Heulin, W. Achouak, and F. e. Z. Haichar “Plant nutrient resource use strategies shape active rhizosphere microbiota through root exudation,” Front. Plant Sci. 9, 1662 (2018). https://doi.org/10.3389/fpls.2018.01662
A. Henry, W. Doucette, J. Norton, and B. Bugbee “Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress,” J. Environ. Qual. 36, 904–912 (2007). https://doi.org/10.2134/jeq2006.0425sc
S. Ishikawa, T. Wagatsuma, R. Sasaki, and P. Ofei-Manu “Comparison of the amount of citric and malic acids in Al media of seven plant species and two cultivars each in five plant species,” Soil Sci. Plant Nutr. 46, 751–758 (2000). https://doi.org/10.1080/00380768.2000.10409141
S. H. Jien and Y. H. Lin “Proteins in Xylem exudates from rapeseed plants (Brassica napus L.) play a crucial role in cadmium phytoremediation,” Clean-Soil Air Water 46, 1700164 (2018). https://doi.org/10.1002/clen.201700164
D. L. Jones “Organic acids in the rhizosphere-a critical review,” Plant Soil 205, 25–44 (1998). https://doi.org/10.1023/a:1004356007312
A. Kusunoki, M. Nanzyo, H. Kanno, and T. Takahashi “Effect of water management on the vivianite content of paddy-rice roots,” Soil Sci. Plant Nutr. 61, 910–916 (2015). https://doi.org/10.1080/00380768.2015.1089787
G. Lv, Y. Kang, L. Li, and S. Wan “Effect of irrigation methods on root development and profile soil water uptake in winter wheat,” Irrigation Science 28, 387–398 (2010). https://doi.org/10.1007/s00271-009-0200-1
L. Ma, Y. Li, P. Wu, X. Zhao, X. Chen, and X. Gao “Effects of varied water regimes on root development and its relations with soil water under wheat/maize intercropping system,” Plant Soil 439, 113–130 (2019). https://doi.org/10.1007/s11104-018-3800-9
M. A. Maqsood, S. Hussain, T. Aziz, and M. Ashraf “Wheat-exuded organic acids Influence zinc release from calcareous soils,” Pedosphere 21, 657–665 (2011). https://doi.org/10.1016/s1002-0160(11)60168-9
P. Marschner and Z. Rengel, “Root exudates and nutrient cycling”, in Nutrient Cycling in Terrestrial Ecosystems, Ed. By N. Günter. (Springer-Verlag, Heidelberg Germany, 2007), pp. 123–157. https://doi.org/10.1007/978-3-540-68027-7_5
A. A. Mergel, A. V. Timchenko, and V. N. Kudeyarov “The role of root exudates in transformation of nitrogen- and carbon-bound compounds in soils,” Eurasian Soil Sci 29, 1151-1155 (1996).
T. O. Ochuodho, E. Olale, V. A. Lantz, J. Damboise, T. L. Chow, F. Meng, J. L. Daigle, and S. Li “Impacts of soil and water conservation practices on potato yield in northwestern New Brunswick, Canada,” J. Soil Water Conserv. 68, 392–400 (2013). https://doi.org/10.2489/jswc.68.5.392
D. Pimentel, B. Berger, D. Filiberto, M. Newton, B. Wolfe, E. Karabinakis, S. Clark, E. Poon, E. Abbett, and S. Nandagopal “Water resources: Agricultural and environmental issues,” Bioscience 54, 909–918 (2004). https://doi.org/10.1641/0006-3568(2004)054[0909:wraaei]2.0.co;2
M. Qiao, J. Xiao, H. Yin, X. Pu, B. Yue, and Q. Liu “Analysis of the phenolic compounds in root exudates produced by a subalpine coniferous species as responses to experimental warming and nitrogen fertilisation,” Chem. Ecol. 30, 555–565 (2014). https://doi.org/10.1080/02757540.2013.868891
J. A. Raven and D. Edwards “Roots: evolutionary origins and biogeochemical significance,” J. Exp. Bot. 52, 381–401 (2001). https://doi.org/10.1093/jexbot/52.suppl_1.381
M. Rodrigues, J. F. T. Gananca, E. M. da Silva, T. M. M. dos Santos, J. J. Slaski, J. Zimny, and M. A. A. Pinheiro de Carvalho “Evidences of organic acids exudation in aluminium stress responses of two Madeiran wheat (Triticum aestivum L.) landraces,” Genet. Resour. Crop Evol. 66, 857–869 (2019). https://doi.org/10.1007/s10722-019-00754-0
H. Sakai, K. Yagi, K. Kobayashi, and S. Kawashima “Rice carbon balance under elevated CO2,” New Phytol. 150, 241–249 (2001). https://doi.org/10.1046/j.1469-8137.2001.00105.x
F. V. Scarpare, Q. d. J. van Lier, L. de Camargo, R. C. M. Pires, S. T. Ruiz-Correa, A. H. F. Bezerra, G. J. C. Gava, and C. T. S. Dias “Tillage effects on soil physical condition and root growth associated with sugarcane water availability,” Soil Till. Res. 187, 110–118 (2019). https://doi.org/10.1016/j.still.2018.12.005
P. A. Seck, A. Diagne, S. Mohanty, and M. C. S. Wopereis “Crops that feed the world 7: Rice,” Food Security 4, 7–24 (2012). https://doi.org/10.1007/s12571-012-0168-1
A. K. Thakur, R. K. Mohanty, D. U. Patil, and A. Kumar “Impact of water management on yield and water productivity with system of rice intensification (SRI) and conventional transplanting system in rice,” Paddy Water Environ. 12, 413–424 (2014). https://doi.org/10.1007/s10333-013-0397-8
T. Thi Hoang Ha and P. Marschner “Addition of residues with different C/N ratio in soil over time individually or as mixes - effect on nutrient availability and microbial biomass depends on amendment rate and frequency,” J. Soil Sci. Plant Nut. 18, 1157–1172 (2018). https://doi.org/10.4067/S0718-95162018005003401
J. Wang, X. Li, J. Zhang, T. Yao, D. Wei, Y. Wang, and J. Wang “Effect of root exudates on beneficial microorganisms-evidence from a continuous soybean monoculture,” Plant Ecol. 213, 1883–1892 (2012). https://doi.org/10.1007/s11258-012-0088-3
P. Wang, R. Zhou, J. Cheng, and S. Bi “LC determination of trace short-chain organic acids in wheat root exudates under aluminum stress,” Chromatographia 66, 867–872 (2007). https://doi.org/10.1365/s10337-007-0418-0
X. Wang, D. Zhu, Y. Wang, X. Wei, and L. Ma “Soil water and root distribution under jujube plantations in the semiarid Loess Plateau region, China,” Plant Growth Regulation 77, 21–31 (2015). https://doi.org/10.1007/s10725-015-0031-4
W. Widodo, J. C. V. Vu, K. J. Boote, J. T. Baker, and L. H. Allen “Elevated growth CO2 delays drought stress and accelerates recovery of rice leaf photosynthesis,” Environ. Exp. Bot. 49, 259–272 (2003). https://doi.org/10.1016/s0098-8472(02)00091-6
F. Wu, F. Xu, X. Ma, W. Luo, L. Lou, and M. H. Wong “Do arsenate reductase activities and oxalate exudation contribute to variations of arsenic accumulation in populations of Pteris vittata?,” J. Soils Sed. 18, 3177–3185 (2018). https://doi.org/10.1007/s11368-018-1987-2
M. Xie, C. Yan, J. Ye, and L. Wei “Impact of phenanthrene on organic acids secretion and accumulation by perennial ryegrass, Lolium perenne L., root,” Bull. Environ. Contam. Toxicol. 83, 75–80 (2009). https://doi.org/10.1007/s00128-009-9775-8
J. Yang “Relationships of Rice Root Morphology and Physiology with the Formation of Grain Yield and Quality and the Nutrient Absorption and Utilization,” Sci Agric Sin 44, 36–46 (2011). (In Chinese)
Y. Yao, F. Zhang, M. Wang, F. Liu, W. Liu, X. Li, D. Qin, X. Geng, X. Huang, and P. Zhang “Thallium-induced oxalate secretion from rice (Oryza sativa L.) root contributes to the reduction of Tl(III) to Tl(I),” Environ. Exp. Bot. 155, 387–393 (2018). https://doi.org/10.1016/j.envexpbot.2018.07.028
H. Yin, Y. Li, J. Xiao, Z. Xu, X. Cheng, and Q. Liu “Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming,” Global Change Biol. 19, 2158–2167 (2013). https://doi.org/10.1111/gcb.12161
A. Zhan, X. Chen, and S. Li “Effects of soil water on maize root morphological and physiological responses to phosphorus supply,” J. Plant Nutr. Soil Sci. 182, 477–484 (2019). https://doi.org/10.1002/jpln.201800160
F. Zhang, V. Romheld, and H. Marschner “Effect of zinc-deficiency in wheat on the release of zinc and iron mobilizing root exudates,” Z. Pflanz. Bodenkunde 152, 205–210 (1989). https://doi.org/10.1002/jpln.19891520211
F. S. Zhang, J. Ma, and Y. P. Cao “Phosphorus deficiency enhances root exudation of low-molecular weight organic acids and utilization of sparingly soluble inorganic phosphates by radish (Raghanus sativus L.) and rape (Brassica napus L.) plants,” Plant Soil 196, 261–264 (1997). https://doi.org/10.1023/a:1004214410785
H. Zhang, Y. Xue, Z. Wang, J. Yang, and J. Zhang “An alternate wetting and moderate soil drying regime improves root and shoot growth in rice,” Crop Sci. 49, 2246–2260 (2009). https://doi.org/10.2135/cropsci2009.02.0099
Funding
This study was funded by the Science and Technology Planning Project of Jilin Province in China (20180520100JH, 20180623026TC) and the Science and Technology Planning Project of the Ministry of Housing and Urban-Rural Development of the People’s Republic of China (2018-K6-003).
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Liang, S., Wang, Y.H., Zhang, H. et al. Response of Root-Exuded Organic Acids in Irrigated Rice to Different Water Management Practices. Eurasian Soil Sc. 53, 1572–1578 (2020). https://doi.org/10.1134/S1064229320110101
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DOI: https://doi.org/10.1134/S1064229320110101