An evaluation on the cold tolerance of twenty-three Cyclocarya paliurus families under natural low temperatures

doi:10.12302/j.issn.1000-2006.202208024

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2024, Vol. 48 ›› Issue (4): 85-92.doi: 10.12302/j.issn.1000-2006.202208024

Special Issue: 专题报道Ⅱ：乡村振兴视域下药用树种青钱柳培育研究

Previous Articles Next Articles

An evaluation on the cold tolerance of twenty-three Cyclocarya paliurus families under natural low temperatures

ZHANG Zanpei¹(), GU Yueying¹, SHANG Xulan¹^,², WANG Ji¹^,³, FANG Shengzuo¹^,²^,^*()

1. College of Forestry and Grassland, Nanjing Forestry University, Nanjing 210037, China
2. Co-Innovation Center for Sustaniable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, China
3. Nanjing Xiaozhuang University, Nanjing 210037, China

Received:2022-08-12 Revised:2023-02-02 Online:2024-07-30 Published:2024-08-05
Contact: FANG Shengzuo E-mail:zhangzanpei@njfu.edu.cn;fangsz@njfu.edu.cn

Abstract

Abstract:

【Objective】To provide a theoretical basis for the introduction, selective breeding, and cultivation of Cyclocarya paliurus, the cold resistance of different families of C. paliurus under natural low temperature stress was evaluated.【Method】Using the current branches of C. paliurus from 23 families as materials, the relative electric conductivity (REC), malondialdehyde (MDA) content, peroxidase (POD) activity, superoxide dismutase (SOD) activity, soluble sugar (SS), soluble protein (SP), starch (ST) and free proline (Pro) content were determined after natural low temperature stress. A preliminary evaluation of the cold resistance of C. paliurus families was conducted through a principal component analysis (PCA) and cluster analysis.【Result】After natural low temperature stress, there were significant differences in the REC, MDA, POD and SOD activity, SS, SP, ST and Pro content among the current branches of the 23 families. The PCA found that the four principal components represented 72.4% of the information regarding the various physiological indicators. A cluster analysis showed that the cold resistance of 23 families could be divided into three categories based on the comprehensive score of the PCA for each family. The first category included only two families (SCMC31 and ZJTTS2) with the good cold resistance, and the compositive score ranging from 1.208 to 1.284. The second category indude 17 families (including GZSQ12, GXBS12, ZJFYS6, AHQLF8 and HBWF10) that exhibited moderate cold resistance, with composite scores ranging from -0.343 to 0.631. The third category included four families (GZSQ9, ZJTTS3, SCMC22, and SCMC30) with poor cold tolerance, with composite scores ranging from -1.259 to -0.745.【Conclusion】After natural low temperature stress, significant differences in the measured physiological indices were observed between the current branches of C. paliurus from different families (P < 0.05). Based on the PCA and cluster analysis results, there were different cold resistances among the 23 Cyclocarya paliurus families, which could be divided into three categories. The results not only provide a basis for an in-depth study of the cold tolerate mechanism of C. paliurus, but also for future screening of the cold tolerate genotypes of C. paliurus.

Key words: Cyclocarya paliurus, family, low temperature stress, principal component analysis(PCA), physiological indicators, overall evaluation

CLC Number:

S725
S718

ZHANG Zanpei, GU Yueying, SHANG Xulan, WANG Ji, FANG Shengzuo. An evaluation on the cold tolerance of twenty-three Cyclocarya paliurus families under natural low temperatures[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(4): 85-92.

Figures/Tables 7

Fig. 1

Fig. 2

Fig. 3

Table 1

Table 2

Table 3

Fig. 4

References 35

[1]	谢明勇, 谢建华. 青钱柳研究进展[J]. 食品与生物技术学报, 2008, 27(1):113-121.
	XIE M Y, XIE J H. Review about the research on Cyclocarya paliurus (Batal.) Iljinskaja[J]. J Food Sci Biotechnol, 2008, 27(1):113-121.DOI: 10.3321/j.issn:1673-1689.2008.01.021.
[2]	方升佐, 洑香香. 青钱柳资源培育与开发利用的研究进展[J]. 南京林业大学学报(自然科学版), 2007, 31(1):95-100.
	FANG S Z, FU X X. Progress and prospects on silviculture and utilization of Cyclocarya paliurus resources[J]. J Nanjing For Univ (Nat Sci Ed), 2007, 31(1):95-100.DOI: 10.3969/j.issn.1000-2006.2007.01.023.
[3]	舒任庚, 徐昌瑞, 黎莲娘. 青钱柳甜味成分的研究[J]. 药学学报, 1995, 30(10):757-761.
	SHU R G, XU C R, LI L N. Studies on the sweet principles from the leaves of Cyclocarya paliurus(Batal.)Iljinsk[J]. Acta Pharm Sin, 1995, 30(10):757-761. DOI: 10.16438/j.0513-4870.1995.10.008.
[4]	钟瑞建, 高幼衡, 徐昌瑞, 等. 青钱柳中五环三萜成分的研究[J]. 中草药, 1996, 27(7):387-388.
	ZHONG R J, GAO Y H, XU C R, et al. Pentacyclic triterpenoids from rounduing fruit Cyclocarya(Cycocarya paliurus)[J]. Chin Tradit Herb Drugs, 1996, 27(7):387-388.
[5]	HE Z W, LV F F, GAN Y L, et al. Anticancer effects of Cyclocarya paliurus polysaccharide (CPP) on thyroid carcinoma in vitro and in vivo[J]. Int J Polym Sci, 2018, 2018:2768120.DOI: 10.1155/2018/2768120.
[6]	HU W B, YANG Z W, WANG W J. Enzymolysis-ultrasonic assisted extraction of flavanoid from Cyclocarya paliurus (Batal.) Iljinskaja:HPLC profile,antimicrobial and antioxidant activity[J]. Ind Crops Prod, 2019, 130:615-626.DOI: 10.1016/j.indcrop.2019.01.027.
[7]	ZHANG L, ZHANG Z J, FANG S Z, et al. Integrative analysis of metabolome and transcriptome reveals molecular regulatory mechanism of flavonoid biosynthesis in Cyclocarya paliurus under salt stress[J]. Ind Crops Prod, 2021, 170:113823.DOI: 10.1016/j.indcrop.2021.113823.
[8]	DING Y, SHI Y, YANG S. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants[J]. New Phytol, 2019, 222(4):1690-1704. DOI: 10.1111/nph.15696.
[9]	权威, 薛文通, 赵天瑶, 等. 植物对低温胁迫的响应机制研究进展[J]. 中国农业大学学报, 2023, 28(2):14-22.
	QUAN W, XUE W T, ZHAO T Y, et al. A review on the response mechanism of plant to low temperature stress[J]. J China Agric Univ, 2023, 28(2):14-22. DOI: 10.11841/j.issn.1007-4333.2023.02.02.
[10]	刘紫烟, 刘佳乐, 朱圆圆, 等. 木本植物低温应答机制研究进展[J]. 西北林学院学报, 2022, 37(2):157-163.
	LIU Z Y, LIU J L, ZHU Y Y, et al. Research process on the the response mechanism of woody plants to low temperature[J]. J Northwest For Univ, 2022, 37(2):157-163. DOI: 10.3969/j.issn.1001-7461.2022.02.21.
[11]	牟开萍, 李维芳, 杨文新, 等. 20个月季品种的抗寒性综合评价[J]. 草原与草坪, 2021, 41(6):58-66.
	MOU K P, LI W F, YANG W X, et al. Comprehensive evaluation on the cold resistance of 20 Rosa chinensis cultivars[J]. Grassland Turf, 2021, 41(6):58-66.DOI: 10.13817/j.cnki.cyycp.2021.06.009.
[12]	刘钰玺, 陈佰鸿, 马宗桓, 等. 河西走廊酿酒葡萄砧木抗寒性综合评价[J]. 甘肃农业大学学报, 2020, 55(6):86-96.
	LIU Y X, CHEN B H, MA Z H, et al. Comprehensive evaluation of cold resistance of grape rootstock in Hexi Corridor[J]. J Gansu Agric Univ, 2020, 55(6):86-96.DOI: 10.13432/j.cnki.jgsau.2020.06.011.
[13]	何伟, 艾军, 范书田, 等. 葡萄品种及砧木抗寒性评价方法研究[J]. 果树学报, 2015, 32(6):1135-1142.
	HE W, AI J, FAN S T, et al. Study on evaluation method for cold resistance of grape cultivars and rootstock[J]. J Fruit Sci, 2015, 32(6):1135-1142.DOI: 10.13925/j.cnki.gsxb.20150150.
[14]	ZHOU W J, LEU L M. Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance,enzyme activities and lipid peroxidation in winter rape[J]. Plant Growth Regul, 1998, 26(1):41-47.DOI: 10.1023/A:1006004921265.
[15]	赵世杰, 许长成, 邹琦, 等. 植物组织中丙二醛测定方法的改进[J]. 植物生理学通讯, 1994, 30(3):207-210.
	ZHAO S J, XU C C, ZOU Q, et al. Improvement of determination method of malondialdehyde in plant tissues[J]. Plant Physiol Commun, 1994, 30(3):207-210.DOI: 10.13592/j.cnki.ppj.1994.03.016.
[16]	AMAKO K, CHEN G X, ASADA K. Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants[J]. Plant Cell Physiol, 1994, 35(3):497-504.DOI: 10.1093/oxfordjournals.pcp.a078621.
[17]	李合生. 植物生理生化实验原理和技术[M]. 北京: 高等教育出版社, 2000:196-197.
	LI H S. Principles and techniques of plant physiological biochemical experiment[M]. Beijing: Higher Education Press, 2000:196-197.
[18]	GIANNOPOLITIS C N, RIES S K. Superoxide dismutases:I.Occurrence in higher plants[J]. Plant Physiol, 1977, 59(2):309-314.DOI: 10.1104/pp.59.2.309.
[19]	ABRAHÁM E, HOURTON-CABASSA C, ERDEI L, et al. Methods for determination of proline in plants[J]. Methods Mol Biol, 2010, 639:317-331.DOI: 10.1007/978-1-60761-702-0_20.
[20]	DING Y L, YANG S H. Surviving and thriving:how plants perceive and respond to temperature stress[J]. Dev Cell, 2022, 57(8):947-958.DOI: 10.1016/j.devcel.2022.03.010.
[21]	SUZUKI N, KOUSSEVITZKY S, MITTLER R, et al. ROS and redox signalling in the response of plants to abiotic stress[J]. Plant Cell Environ, 2012, 35(2):259-270.DOI: 10.1111/j.1365-3040.2011.02336.x.
[22]	NADARAJAH K K. ROS homeostasis in abiotic stress tolerance in plants[J]. Int J Mol Sci, 2020, 21(15):5208.DOI: 10.3390/ijms21155208.
[23]	DRAPER H H, HADLEY M. Malondialdehyde determination as index of lipid Peroxidation[M]// Oxygen Radicals in Biological Systems Part B: Oxygen Radicals and Antioxidants. Amsterdam:Elsevier, 1990:421-431.DOI: 10.1016/0076-6879(90)86135-i.
[24]	徐亚军, 赵龙飞, 邢鸿福, 等. 内生细菌对盐胁迫下小麦幼苗脯氨酸和丙二醛的影响[J]. 生态学报, 2020, 40(11):3726-3737.
	XU Y J, ZHAO L F, XING H F, et al. Effects of endophytic bacteria on proline and malondialdehyde of wheat seedlings under salt stress[J]. Acta Ecol Sin, 2020, 40(11):3726-3737.DOI: 10.5846/stxb201802060309.
[25]	GONG Z Z, XIONG L M, SHI H Z, et al. Plant abiotic stress response and nutrient use efficiency[J]. Sci China Life Sci, 2020, 63(5):635-674.DOI: 10.1007/s11427-020-1683-x.
[26]	HUANG Z, ZHAO N, QIN M F, et al. Mapping of quantitative trait loci related to cold resistance in Brassica napus L[J]. J Plant Physiol, 2018, 231:147-154.DOI: 10.1016/j.jplph.2018.09.012.
[27]	PONTIS H G. Fructans and cold stress[J]. J Plant Physiol, 1989, 134(2):148-150.DOI: 10.1016/s0176-1617(89)80047-1.
[28]	GUY C L, HUBER J L, HUBER S C. Sucrose phosphate synthase and sucrose accumulation at low temperature[J]. Plant Physiol, 1992, 100(1):502-508.DOI: 10.1104/pp.100.1.502.
[29]	YAMADA M, MORISHITA H, URANO K, et al. Effects of free proline accumulation in petunias under drought stress[J]. J Exp Bot, 2005, 56(417):1975-1981.DOI: 10.1093/jxb/eri195.
[30]	李晓龙, 褚燕南, 张磊, 等. 苹果花期抗寒能力判定指标解析[J]. 果树学报, 2022, 39(10):1935-1944.
	LI X L, CHU Y N, ZHANG L, et al. Analysis of evaluation indexes of cold resistance of apple trees at flowering stage[J]. J Fruit Sci, 2022, 39(10):1935-1944.DOI: 10.13925/j.cnki.gsxb.20210704.
[31]	张博, 刘立强, 秦伟, 等. 新疆野苹果抗寒生理生化机制研究[J]. 经济林研究, 2021, 39(4):60-68.
	ZHANG B, LIU L Q, QIN W, et al. Study on physiological and biochemical mechanism of cold resistance of Malus sieversii[J]. Non Wood For Res, 2021, 39(4):60-68.DOI: 10.14067/j.cnki.1003-8981.2021.04.008.
[32]	韩立群, 马凯, 丁军伟, 等. 低温处理下新疆野生核桃的生理响应及抗寒性评价[J]. 西北林学院学报, 2019, 34(5):98-101,126.
	HAN L Q, MA K, DING J W, et al. Physiological response and evaluation of cold resistance of Xinjiang wild walnut under low temperature stress[J]. J Northwest For Univ, 2019, 34(5):98-101,126.DOI: 10.3969/j.issn.1001-7461.2019.05.15.
[33]	吴硕, 贾彦丽, 智福军. 低温胁迫下核桃枝条抗寒性综合评价[J]. 林业与生态科学, 2020, 35(3):314-319.
	WU S, JIA Y L, ZHI F J. Comprehensive evaluation of cold resistance of walnut branches under low temperature stress[J]. For Ecol Sci, 2020, 35(3):314-319.DOI: 10.13320/j.cnki.hjfor.2020.0042.
[34]	王一峰, 赵淑玲, 王瀚, 等. 不同核桃种质展叶期抗寒性的综合评价[J]. 经济林研究, 2019, 37(1):50-60.
	WANG Y F, ZHAO S L, WANG H, et al. Comprehensive evaluation on cold resistance of different walnut germplasms at leaf-expansion period[J]. Non Wood For Res, 2019, 37(1):50-60.DOI: 10.14067/j.cnki.1003-8981.2019.01.008.
[35]	WISNIEWSKI M, NASSUTH A, TEULIÈRES C, et al. Genomics of cold hardiness in woody plants[J]. Crit Rev Plant Sci, 2014, 33(2/3):92-124.DOI: 10.1080/07352689.2014.870408.

Related Articles 15

[1]	LIU Xiaofang, YUE Xiliang, FANG Shengzuo, LI Qing, SUN Xin. Effects of various ratios of nitrogen and phosphorus addition on the growth and contents of leaf bioactive substances in Cyclocarya paliurus [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(4): 57-66.
[2]	LIU Li, QU Yinquan, YU Yanhao, WANG Qian, FU Xiangxiang. Analysis of SSR locus based on the whole genome sequences of Cyclocarya paliurus and the development of polymorphic primers [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(4): 67-75.
[3]	LIU Xialan, SONG Ziqi, HU Fengrong, SHANG Xulan. A comparative study on leaf characters between diploid and tetraploid of Cyclocarya paliurus [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(4): 76-84.
[4]	ZHAO Zhiqiang, XU Xiaolong, YUAN Qing, WU Yan. Landscape pattern evolution and driving factors of Songhua River wetland in Harbin [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(2): 219-226.
[5]	SONG Ziqi, BIAN Guoliang, LIN Feng, HU Fengrong, SHANG Xulan. Establishment and application of a flow cytometry method for chromosome ploidy identification of Cyclocarya paliurus [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(2): 61-68.
[6]	WANG Ji, FANG Shengzuo. Effects of different anti-browning agents on enzyme activity and growth in callus of Cyclocarya paliurus [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2023, 47(6): 167-174.
[7]	HUANG Ziliang, XU Ziheng, SUN Caowen. Study on seasonal dynamics of seed rain and characteristics of soil seed banks in Cyclocarya paliurus [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2023, 47(2): 18-26.
[8]	WANG Wenyue, ZHANG Zhen, JIN Guoqing, SUN Linshan, QIU Yongbin, ZHOU Zhichun, YANG Tao. Family variation and selection of growth traits of eight-year-old Cupressus funebris in two sites [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2023, 47(2): 42-48.
[9]	FANG Shengzuo. A review on the development history and the resource silviculture of Cyclocarya paliurus industry [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(6): 115-126.
[10]	JIA Qingbin, LIU Geng, ZHAO Jiali, LI Kuiyou, SUN Wensheng. Variation analyses of growth traits in half-sib families of Korean pine and superior families selection [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(4): 109-116.
[11]	LI Dandan, WENG Qijie, GAN Siming, ZHOU Changpin, HUANG Shineng, LI Mei. Identification of full-sib seedlings from an open-pollinated family of Archidendron clypearia based on EST-SSR markers [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(4): 95-101.
[12]	XU Zhanhong, ZHU Ying, JIN Huiying, SUN Caowen, FANG Shengzuo. Variations in the contents of leaf pigments and polyphenols and photosynthesis traits in Cyclocarya paliurus with different leaf colors [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(2): 103-110.
[13]	WANG Zhanjun, WU Ziqi, WANG Zhaoxia, OU Zulan, LI Jie, CAI Qianwen, XU Zhongdong, ZHANG Zhaoliang. A comparative study of the evolution and codon usage bias in WOX gene family of three Camellia sinensis cultivars [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(2): 71-80.
[14]	SUN Caowen, ZHONG Wenwen, FU Xiangxiang, SHANG Xulan, FANG Shengzuo. A study on growth and aboveground biomass production of juvenile Cyclocarya paliurus plantations [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(1): 138-144.
[15]	ZHANG Heng, CUI Mengran, SHAN Yanlong, WANG Fei. Study on flammability of herbaceous fuel in typical grassland of China-Mongolia border [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2021, 45(5): 171-177.

Metrics

Comments

www.nldxb.njfu.edu.cn

Edited ＆ Published by Editorial Department of Nanjing Forestry University(Natural Sciences Edition)
Address： No.159 Longpan Road,Nanjing 210037 Jiangsu,P.R.China
E-mail ：xuebao@njfu.edu.cn , xuebao@njfu.com.cn
Telephone +86-25-85428247,85427076
Distributed by China International Book Trading Corporation P.O. Box 399, Beijing ,P.R. China

家系 family	可溶性糖含量/(mg·g^-1) soluble sugar content	可溶性蛋白含量/(mg·g^-1) soluble protein content	淀粉含量/(mg·g^-1) starch content	游离脯氨酸含量/(μg·g^-1) free proline content
AHJD1	11.19±0.63 defg	4.56±0.31 f	3.70±1.31 abcdef	128.53±3.35 g
AHQLF3	15.63±1.23 a	2.44±0.16 jk	4.72±1.15 ab	66.13±1.67 k
AHQLF8	11.32±0.72 cdefg	4.70±0.26 f	3.26±0.68 bcdef	175.73±1.62 e
AHQLF16	10.96±0.50 defgh	4.00±0.33 gh	3.76±0.79 abcde	174.53±4.20 e
GXBS12	11.92±0.49 cde	4.15±0.10 g	4.96±1.34 a	93.07±2.72 i
GXJZS1	10.11±1.12 efgh	3.80±0.18 gh	2.77±0.18 def	101.60±1.20 h
GZJH15	9.46±0.15 gh	3.99±0.13 gh	4.21±1.07 abcd	159.87±0.61 f
GZLP4	11.28±0.36 cdefg	5.21±0.24 e	4.13±0.20 abcd	224.40±13.51 c
GZSQ9	12.50±0.55 bcd	3.58±0.15 h	3.12±0.26 cdef	34.53±0.61 n
GZSQ12	13.34±2.35 bc	6.64±0.28 bc	3.79±0.21 abcde	164.40±1.20 f
HBWF10	12.99±2.33 bcd	5.71±0.40 d	3.49±0.44 abcdef	391.60±6.68 b
HBWF15	9.69±1.05 fgh	3.64±0.06 h	4.38±0.08 abc	57.07±2.54 l
SCMC22	11.23±1.31 cdefg	3.14±0.23 i	2.25±0.30 f	190.00±3.42 d
SCMC30	8.94±0.46 h	1.95±0.12 l	3.12±0.96 cdef	158.13±1.89 f
SCMC31	16.01±1.64 a	6.99±0.34 ab	4.42±0.88 abc	413.20±3.67 a
ZJFYS2	14.33±0.86 ab	4.01±0.28 gh	2.45±0.44 ef	162.53±8.09 f
ZJFYS6	11.97±1.15 cde	7.27±0.30 a	3.47±0.27 abcdef	45.87±1.01 m
ZJLWS3	11.74±0.72 cdef	2.15±0.08 kl	4.52±1.05 abc	58.60±1.00 l
ZJMWL4	9.67±0.65 fgh	6.47±0.46 c	3.15±0.42 cdef	70.80±2.40 k
ZJSLG9	12.10±0.35 cde	5.29±0.28 e	3.29±0.77 bcdef	36.00±0.40 n
ZJTTS2	15.96±1.61 a	6.59±0.31 bc	4.63±0.50 abc	83.73±2.20 j
ZJTTS3	10.97±0.43 defgh	2.48±0.12 jk	2.61±0.54 ef	33.87±0.23 n
ZJWC1	12.30±0.54 cd	2.68±0.13 j	4.17±1.23 abcd	134.60±1.00 g

主成分 principal component	特征根 eigenvalue	贡献率/% contribution rate	累积贡献率/% cumulative contribution rate
1	1.703	21.292	21.292
2	1.542	19.274	40.566
3	1.420	17.746	58.312
4	1.127	14.086	72.398

生理指标 physiological indicator	主成分principal component
生理指标 physiological indicator	1	2	3	4
可溶性蛋白含量 soluble protein content	0.770	0.067	0.028	0.417
相对电导率 relative electric conductivity	-0.725	-0.323	0.195	0.092
游离脯氨酸含量 free proline content	0.627	0.024	-0.541	-0.163
淀粉含量 starch content	0.108	0.747	0.366	-0.024
丙二醛含量 malondialdehyde content	0.033	0.735	-0.453	0.027
可溶性糖含量 soluble sugar content	0.385	0.574	-0.169	-0.085
过氧化物酶活性 peroxidase activity	-0.169	-0.056	0.846	-0.104
超氧化物歧化酶活性 superoxide dismutase activity	0.034	-0.053	-0.066	0.948

An evaluation on the cold tolerance of twenty-three Cyclocarya paliurus families under natural low temperatures

RichHTML

PDF

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 7

References 35

Related Articles 15

Recommended Articles

Metrics

Comments

Author

Reader

Reviewer