Identification and expression analysis of PAL gene family in apple

doi:10.3969/j.issn.1004-1524.2018.12.07

›› 2018, Vol. 30 ›› Issue (12): 2031-2043.DOI: 10.3969/j.issn.1004-1524.2018.12.07

• Horticultural Science • Previous Articles Next Articles

Identification and expression analysis of PAL gene family in apple

ZHANG Lizhi, FAN Sheng, AN Na, ZUO Xiya, GAO Cai, ZHANG Dong^*, HAN Mingyu

College of Horticulture, Northwest A&F University, Yangling 712100, China

Received:2018-03-09 Online:2018-12-25 Published:2018-12-28

Abstract

Abstract: Based on apple genome and the genomic database of Golden Delicious, 8 apple PAL genes were identified through BLAST tool. All members shared conserved MIO active site including Ala-Gly-Ser. The analysis of classification and evolutionary relationship showed that the 8 MdPAL genes were divided into three groups, the molecular weight was between 47.713 and 81.748 ku, the isoelectric point was between 5.44 and 6.39, and the members of one subgroup shared similar gene structure and conserved protein motifs. Based on GEO database and qRT-PCR, expression patterns of MdPAL genes in different organs and different stages of fruits in Nagafu No.2 were determined. The analysis of expression patterns of MdPAL genes in different organs showed that MdPAL2, MdPAL3/4/6/7, MdPAL8 had the highest expression levels in leaves, while MdPAL1 and MdPAL5 expressions were the highest in flowers. The expression patterns were diverse. In 5 stages of the fruit development in Nagafu No.2, the expression patterns of MdPAL genes were significantly increased in the young stage or the ripening stage except MdPAL1, indicating that they might play important roles in different stages during the fruit development.

Key words: apple, PAL gene family, bioinformatics, phylogenetic analysis, gene expression

CLC Number:

S661.1

ZHANG Lizhi, FAN Sheng, AN Na, ZUO Xiya, GAO Cai, ZHANG Dong, HAN Mingyu. Identification and expression analysis of PAL gene family in apple[J]. , 2018, 30(12): 2031-2043.

References

[1] FRASER C M, CHAPPLE C.The phenylpropanoid pathway in Arabidopsis[J]. Arabidopsis Book, 2011, 9: e0152.
[2] KOUKOL J, CONN E E.Metabolism of aromatic compounds in higher plants. Ⅳ. Purification and properties of phenylalanine deaminase of Horden vulgare[J]. Journal of Biological Chemistry, 1961, 236(10): 2692-2698.
[3] JOOS H, HAHLBROCK K.Phenylalanine ammonia-lyase in potato (Solanum tuberosum L.): genomic complexity, structural comparison of 2 selected genes and modes of expression[J]. European Journal of Biochemistry, 1992, 204(2): 621-629.
[4] WHETTEN R W, SEDEROFF R R.Phenylalanine ammonia-lyase from loblolly pine: purification of the enzyme and isolation of complementary DNA clones[J]. Plant Physiology, 1992, 98(1): 380-386.
[5] HAMBERGER B, ELLIS M F M, SOUZA C D A, et al. Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families[J]. Canadian Journal of Botany, 2007, 85(12):1182-1201.
[6] CHANG A, LIM M H, LEE S W, et al.Tomato phenylalanine ammonia-lyase gene family, highly redundant but strongly underutilized[J]. Journal of Biological Chemistry, 2008, 283(48): 33591.
[7] REICHERT A I, HE X Z, DIXON R A.Phenylalanine ammonia-lyase (PAL) from tobacco (Nicotiana tabacum): characterization of the four tobacco PAL genes and active heterotetrameric enzymes[J]. Biochemical Journal, 2009, 424(2): 233-242.
[8] 孙润泽, 张雪, 成果, 等. 葡萄苯丙氨酸解氨酶基因家族的全基因组鉴定及表达分析[J].植物生理学报, 2016, 52(2): 195-208.
SUN R Z, ZHANG X, CHENG G, et al.Genome-wide characterization and expression analysis of the phenylalanine ammonia-lyase gene family in grapevine (Vitis vinifera L.)[J]. Plant Physiology Communications, 2016, 52(2): 195-208. (in Chinese with English abstract)
[9] RITTER H, SCHULZ G E.Structural basis for the entrance into the phenylpropanoid metabolism catalyzed by phenylalanine ammonia-lyase[J]. Plant Cell, 2004, 16(12): 3426-3436.
[10] 徐晓梅, 杨署光. 苯丙氨酸解氨酶研究进展[J]. 安徽农业科学, 2009,37(31): 15115-15119.
XU X M, YANG S G.Advances in the studies of phenylalanine ammonia-lyase[J]. Journal of Anhui Agricultural Sciences, 2009, 37(31): 15115-15119. (in Chinese with English abstract)
[11] SANTIAGO R, ARMAS R D, LEGAZ M E, et al.Changes in phenolic acids content, phenylalanine ammonia-lyase and peroxidase activities in sugarcane leaves induced by elicitors isolated from Xanthomonas albilineans[J]. Australasian Plant Pathology, 2009, 38(4): 357-365.
[12] GALLÃO M I, CORTELAZZO Â L, FEVEREIRO M P S, et al. Biochemical and morphological responses to abiotic elicitor chitin in suspension-cultured sugarcane cells[J]. Brazilian Archives of Biology & Technology, 53(2): 253-260.
[13] 樊胜, 张晓晓, 周会玲,等. 紫外线照射对采后苹果抗灰霉病作用的研究[J]. 西北农林科技大学学报(自然科学版), 2016, 44(2): 172-178.
FAN S, ZHANG X X, ZHOU H L, et al.Effect of UV-C irradiation on gray mold of postharvest apples[J]. Journal of Northwest A & F University (Natural Science Edition), 2016, 44(2): 172-178. (in Chinese with English abstract)
[14] VILJOEN M M, HUYSAMER M.Biochemical and regulatory aspects of anthocyanin synthesis in apples and pears[J]. Journal of Southern African Society for Horticultural Sciences, 1995, 29(3): 307-311.
[15] BLANKENSHIP S M, UNRATH C R.PAL and ethylene content during maturation of red and golden delicious apples[J]. Phytochemistry, 1988, 27(4): 1001-1002.
[16] KUBO Y, TAIRA S, ISHIO S, et al.Color development of 4 apple cultivars grown in the southwest of japan, with special reference to fruit bagging[J]. Engei Gakkai Zasshi, 1988, 57(2): 191-199.
[17] CHENG G, HE Y N, YUE T X, et al.Effects of climatic conditions and soil properties on cabernet sauvignon berry growth and anthocyanin profiles[J]. Molecules, 2014, 19(9): 13683-13703.
[18] ADAMS D O.Phenolics and ripening in grape berries[J]. American Journal of Enology & Viticulture, 2006, 57(3): 249-256.
[19] CHEN J Y, WEN P F, KONG W F, et al.Changes and subcellular localizations of the enzymes involved in phenylpropanoid metabolism during grape berry development[J]. Journal of Plant Physiology, 2006, 163(2): 115-127.
[20] BRAIDOT E, ZANCANI M, PETRUSSA E, et al.Transport and accumulation of flavonoids in grapevine (Vitis vinifera L.)[J]. Plant Signaling & Behavior, 2008, 3(9): 626-632.
[21] 聂继云, 吕德国, 李静,等. 苹果果实中类黄酮化合物的研究进展[J]. 园艺学报, 2009, 36(9):1390-1397.
NIE J Y, LYU D G, LI J, et al.Advances in studies on flavonoids in apple fruit[J]. Acta Horticulturae Sinica, 2009, 36(9): 1390-1397. (in Chinese with English abstract)
[22] TEIXEIRA A, EIRASDIAS J, CASTELLARIN S D, et al.Berry phenolics of grapevine under challenging environments[J]. International Journal of Molecular Sciences, 2013, 14(9): 18711.
[23] LISTER C E, LANCASTER J E, WALKER J R L. Phenylalanine ammonia-lyase (PAL) activity and its relationship to anthocyanin and flavonoid levels in new zealand-grown apple cultivars[J]. American Society for Horticultural Science, 1996, 121(2): 281-285.
[24] VELASCO R, ZHARKIKH A, PRUSS D, et al.The genome of the domesticated apple (Malus × domestica Borkh.)[J]. Nature Genetics, 2010, 42(10): 833.
[25] FAN S, ZHANG D, XING L B, et al.Phylogenetic analysis of IDD gene family and characterization of its expression in response to flower induction in Malus[J]. Molecular Genetics & Genomics, 2017, 292(4): 755-771.
[26] 郭梦月, 党美乐, 杨亚州, 等. 苹果新品种‘瑞阳’果实主要特性研究[J]. 西北植物学报,2017, 37(12):2460-2466.
GUO M Y, DANG M L, YANG Y Z, et al.Study of the main fruit characteristics of new apple variety ‘Ruiyang'[J]. Acta Botanica Boreali-Occidentalia Sinica, 2017,37(12):2460-2466. (in Chinese with English abstract)
[27] CHU Z, WANG X, LI Y, et al.Genomic organization, phylogenetic and expression analysis of the B-BOX gene family in tomato[J]. Frontiers in Plant Science, 2016, 7: 1552.
[28] 许园园, 蔺经, 李晓刚, 等. 梨CBL基因家族全基因组序列的鉴定及非生物胁迫下的表达分析[J]. 中国农业科学, 2015, 48(4): 735-747.
XU Y Y, LIN J, LI X G, et al.Identification and expression analysis under abiotic stresses of the CBL gene family in pear[J]. Scientia Agricultura Sinica, 2015, 48(4): 735-747. (in Chinese with English abstract)
[29] HUNTER S, APWEILER R, BINNS D, et al.ExPASy: SIB bioinformatics resource portal[J]. Nucleic Acids Research, 2012, 40(W1): W597-W603.
[30] 刘仁虎,孟金陵. MapDraw:在Excel中绘制遗传连锁图的宏[J].遗传,2003,25(3):317-321.
LIU R H, MENG J L.MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data[J]. Hereditas(Beijing), 2003, 25(3): 317-321. (in Chinese with English abstract)
[31] LI J, HOU H, LI X, et al.Genome-wide identification and analysis of the SBP-BOX family genes in apple (Malus × domestica Borkh)[J]. Plant Physiology and Biochemistry, 2013, 70: 100-114.
[32] FAN S, ZHANG D, ZHANG L Z, et al.Comprehensive analysis of GASA family members in the Malus domestica genome: identification, characterization, and their expressions in response to apple flower induction[J]. BMC Genomics, 2017, 18(1): 827.
[33] 邵红霞, 陈鸿飞, 张东, 等.苹果YABBY基因家族的鉴定、进化及表达分析[J]. 浙江农业学报, 2017, 29(7): 1129-1138.
SHAO H X, CHEN H F, ZHANG D, et al.Identification, evolution and expression analysis of the YABBY gene family in apple (Malus×domestica Borkh.)[J]. Acta Agriculturae Zhejiangensis, 2017, 29(7): 1129-1138. (in Chinese with English abstract)
[34] YANG S, ZHANG X, YUE J X, et al.Recent duplications dominate NBS-encoding gene expansion in two woody species[J]. Molecular Genetics & Genomics, 2008, 280(3): 187-198.
[35] GEOURJON C, DELÉAGE G. SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments[J]. Bioinformatics, 1995, 11(6): 681-684.
[36] KELLEY L A, MEZULIS S, YATES C M, et al.The PHYRE2 web portal for protein modeling, prediction and analysis[J]. Nature Protocols, 2015, 10(6), 845-858.
[37] TAMURA K, STECHER G, PETERSON D, et al.MEGA6: molecular evolutionary genetics analysis version 6.0[J]. Molecular Biology & Evolution, 2013, 30(12): 2725-2729.
[38] HU B, JIN J, GUO A Y, et al.GSDS 2.0: an upgraded gene feature visualization server[J]. Bioinformatics, 2015, 31(8): 1296-1297.
[39] BAILEY T L, WILLIAMS N, MISLEH C, et al.MEME: discovering and analyzing DNA and protein sequence motifs[J]. Nucleic Acids Research, 2006, 34(Suppl.): W369-W373.
[40] POSTEL D, VANLEMMENS P, GODE P, et al.PLANTCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences[J]. Nucleic Acids Research, 2002, 30(1): 325-327.
[41] GAMBINO G, PERRONE I, GRIBAUDO I.A Rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants[J]. Phytochemical Analysis, 2008, 19(6): 520-525.
[42] FAN S, ZHANG D, LEI C, et al.Proteome analyses using iTRAQ labeling reveals critical mechanisms in alternate bearing Malus prunifolia[J]. Journal of Proteome Research, 2016, 15(10):3602-3616.
[43] LIVAK K J, SCHMITTGEN T D.Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method[J]. Methods, 2001, 25(4): 402-408.
[44] BARRETT T, WILHITE S E, LEDOUX P, et al.NCBI GEO: archive for functional genomics data sets: update[J]. Nucleic Acids Research, 2013, 41(D1):D991-D995.

Identification and expression analysis of PAL gene family in apple

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	ZHANG Jun, ZHANG Bo, HU Bibo, LIU Jingliang, ZHANG Xiaoyu, LI Chunyang, XIONG Shengting, GUO Binbin, WANG Xiucun, MA Chao. Identification and expression analysis of members of the SWEET and SUT families in wheat (Triticum aestivum L.) [J]. Acta Agriculturae Zhejiangensis, 2025, 37(9): 1825-1839.
[2]	QI Yingji, LIU Shuya, LAN Hanyun, WANG Xuemei, SUN Tiantian, LI Shuhan, LI Qiunan, HUANG Xiaoli, GENG Yi, CHEN Defang, OUYANG Ping. Isolation, identification and genome-wide analysis of Spring viremia of carp virus in Sichuan Province of China [J]. Acta Agriculturae Zhejiangensis, 2025, 37(7): 1430-1440.
[3]	DI Yancui, JI Zelin, WANG Yuanyuan, LOU Shihao, ZHANG Tao, GUO Zhixin, SHEN Shunshan, PIAO Fengzhi, DU Nanshan, DONG Xiaoxing, DONG Han. Identification, subcellular localization and expression analysis of tomato SlMYB52 gene [J]. Acta Agriculturae Zhejiangensis, 2025, 37(4): 808-819.
[4]	ZHANG Meiying, MO Qian, QI Xiushuang, TONG Ningning, KONG Fan, LIU Zheng’an, LYU Changping, PENG Liping. Cloning and expression analysis of peony PoLPAT2 gene [J]. Acta Agriculturae Zhejiangensis, 2025, 37(2): 321-328.
[5]	CUI Bowen, ZHANG Siyi, WANG Jialing, WANG Jinghong, LIN Jixiang, YANG Qingjie. Bioinformatics analysis and drought-tolerant gene mining of WRKY family members in Carex siderosticta [J]. Acta Agriculturae Zhejiangensis, 2025, 37(10): 2087-2103.
[6]	JIANG Wenjun, SHU Hongsuo, CHEN Zhengman, REN Dianting, YANG Dang, TIAN Rongjiang, DU Zhaokui. Cloning, expression, and bioinformatics analysis of KoWRKY43 gene in Kandelia obovata [J]. Acta Agriculturae Zhejiangensis, 2024, 36(8): 1832-1843.
[7]	HE Changxi, ZHENG Jianbo, MA Jianbo, JIA Yongyi, LIU Shili, JIANG Wenping, CHI Meili, CHENG Shun, LI Fei. Cloning and expression analysis of Runx2b in Culter alburnus [J]. Acta Agriculturae Zhejiangensis, 2024, 36(5): 1024-1031.
[8]	LI Yaping, JIN Fulai, HUANG Zonggui, ZHANG Tao, DUAN Xiaojing, JIANG Wu, TAO Zhengming, CHEN Jiadong. Identification and expression pattern analysis of glycoside hydrolase GH3 gene family in Dendrobium officinale [J]. Acta Agriculturae Zhejiangensis, 2024, 36(4): 790-799.
[9]	ZHANG Luhe, WANG Duofeng, ZHANG De, ZHANG Guangzhong, ZHAO Tong, LYU Binyan, ZHANG Yangjun, LI Yi. Identification and bioinformatics analysis of novel-miR16 target gene ZjTCP4 in Chinese jujube [J]. Acta Agriculturae Zhejiangensis, 2024, 36(3): 534-543.
[10]	PENG Jiacheng, WU Yue, XU Jiehao, XIA Meiwen, QI Tianpeng, XU Haisheng. Cloning of paxillin gene from Macrobrachium nipponense and effect of cadmium stress on its expression [J]. Acta Agriculturae Zhejiangensis, 2024, 36(2): 247-253.
[11]	LIU Xiaolin, SUN Tingting, YANG Jie, HE Hengbin. Cloning and expression analysis of FLS gene of flavonol synthetase in Lilium auratum and L.speciosum var. gloriosoides [J]. Acta Agriculturae Zhejiangensis, 2024, 36(2): 344-357.
[12]	ZHAO Lingji, LIAO Xiangjiao, LIU Dechun, HU Wei, KUANG Liuqing, SONG Jie, YI Mingliang, LIU Yong, YANG Li. Changes of organic acid content in Taoxi pomelo fruits during the storage period and citric acid related gene expression analysis [J]. Acta Agriculturae Zhejiangensis, 2024, 36(11): 2510-2520.
[13]	ZHANG Li, WANG Yuanyuan, WANG Rui, LIU Lixia. Cloning sequencing and bioinformatics analysis of DRA gene of yak [J]. Acta Agriculturae Zhejiangensis, 2023, 35(7): 1564-1570.
[14]	CUI Yuzhao, YAN Dongyun, WANG Wenhao, TAN Huiting, SUN Wei. Effects of different calcium preparations on postharvest storage quality of Yanfu 3 apple fruit [J]. Acta Agriculturae Zhejiangensis, 2023, 35(7): 1582-1590.
[15]	SHOU Weisong, HE Yanjun, SHEN Jia, XU Xinyang. Genome-wide identification and bioinformatics analysis of SWEET gene family in melon [J]. Acta Agriculturae Zhejiangensis, 2023, 35(7): 1591-1603.