Studies on Mechanisms of ALA Alleviating ABA Inhibiting Root Growth of Strawberry

doi:10.16420/j.issn.0513-353x.2021-1215

Acta Horticulturae Sinica ›› 2023, Vol. 50 ›› Issue (3): 461-474.doi: 10.16420/j.issn.0513-353x.2021-1215

• Research Papers • Next Articles

Studies on Mechanisms of ALA Alleviating ABA Inhibiting Root Growth of Strawberry

RAO Zhixiong¹, AN Yuyan¹, CAO Rongxiang², TANG Quan², WANG Liangju¹^,^*()

¹College of Horticulture，Nanjing Agricultural University，Nanjing 210095，China
²Institute of Agricultural Sciences in Jiangsu Hilly Area，Nanjing 210046，China

Received:2022-08-17 Revised:2022-11-04 Online:2023-03-25 Published:2023-04-03
Contact: *（E-mail：wlj@njau.edu.cn）

Abstract

Abstract:

The relationship among 5-aminolevulinic acid（ALA），abscisic acid（ABA）and auxin （IAA）in strawberry roots growth were discussed. It was found that exogenous ABA treatment significantly inhibited strawberry root growth，while ALA alleviated the inhibitory effect by ABA. ABA reduced the endogenous IAA content in the root tips of strawberry，while ALA promoted endogenous ABA content. The expressions of NCED1，NCED2 and CYP707A，referring to ABA biosynthesis and catabolism，respectively，were not different among treatments，whereas that of PYL4 and PYL8，both coding ABA receptors，and SnRK2.1，SnRK2.2，SnRK2.3，SnRK2.4，SnRK2.5 and SnRK2.6，which code the protein kinases in ABA signaling pathway were up-regulated by ABA but not mediated by ALA. These results suggested that the genes in ABA signaling route were not involved in ALA-ABA regulating root growth of strawberry. On the other hand，ABA down-regulated expressions of YUC2，YUC3（referring to IAA synthesis） and AUX1（coding auxin influx carrier）. However，the down-regulation of gene expressions by ABA were not reversed by ALA. This also means that these genes are not so important in ALA-ABA-regulated root growth of strawberry. Nevertheless，the expression of PIN1，which codes IAA exporter carrier，was down-regulated by ABA，and ALA reversed the down-regulation，suggesting that PIN1 may be involved in ALA-ABA regulating root growth of strawberry. In a transgenic Arabidopsis carrying the green fluorescent protein gene（GFP），it was found that AtPIN1-GFP expression was inhibited by ABA and reversed by ALA. Bioinformatic analysis showed that the amino acid sequence of FaPIN1 in the cultivated strawberry is high homology with many Rosaceous plants，with several transmembrane regions located at both ends of the polypeptide. When FaPIN1-GFP was transferred into tobacco （Nicotiana benthamiana），the fluorescence was distributed in the plasma membrane. When the cloned FaPIN1 was constructed into an estradiol-induced expression vector and transformed into Arabidopsis，the root growth of the transgenic plants was less sensitive to ABA treatment，and the ALA mitigation was also less significant. These results suggest that FaPIN1 is an important factor during ALA-ABA regulating root growth，and the alleviation of ALA on ABA-inhibiting root growth may be dependent on the promotion of IAA polar transport in the root tip of strawberry.

Key words: Fragaria × ananassa, root, growth, 5-aminolevulinic acid, ABA, auxin

CLC Number:

S668.4

RAO Zhixiong, AN Yuyan, CAO Rongxiang, TANG Quan, WANG Liangju. Studies on Mechanisms of ALA Alleviating ABA Inhibiting Root Growth of Strawberry[J]. Acta Horticulturae Sinica, 2023, 50(3): 461-474.

Figures/Tables 10

Table 1 The primers for RT-qPCR analysis of strawberry roots

引物名称 Primer name	正向序列（5′-3′） Forward primer	反向序列（5′-3′） Reverse primer
ACTIN	F-TGGGTTTGCTGGAGATGAT	R-GAGTTAGGAGAACTGGGTGC
YUCCA1	F-GAAAGGTGAGCGTGGGTTA	R-TATGGCGACGACGATAGAG
YUCCA2	F-CTCCGTCTTCATCTCCCTAA	R-CAAACGTACTCAATCTCCTCC
YUCCA3	F-CTTGTCGTCGGTTGTGGAA	R-GCCTGTTGAGCCCGTATTT
AUX1	F-CTGGTTAGCTTCACGGTCTA	R-GAACTCTTAGCGATGTGGG
PIN1	F-GGGAAAGTGGAGGGTAGAAGA	R-TGCCACCTGTAGGATACGAGA
CYP707A	F-AGACGTGGAGTTTGAGGGTT	R-TAGTTGTGAGGTGGTGGAGG
NCED1	F-AGTCCGACGAGGTTGTTGTG	R-CCGAGTCTTTCTACCGAGCAG
NCED2	F-TTATCTCGCCATTGCTGAAC	R-GAAGGAAGAAAGAAAGGCTCAC
PYL4	F-CAACCCACAAGCCTACAAGCA	R-TCGTGACGGAGCGGTAGTTC
PYL8	F- CATACTACTGCCTGTCTGTC	R-GGATGAAACCTGCTACTT
SnRK2.1	F-ATTCACAACCCAAATCAACT	R-ACATCTGCTATCTTCCCATC
SnRK2.2	F-ATCCTTACTGTACGCTACGC	R-ACTTCCTCCTTCCTTCATTT
SnRK2.3	F-ACCACAATAATTTCACCACCAT	R-ACCTACCAAGATTCCGAGCT
SnRK2.4	F-TCTTGAATCGGGTTTCTTGT	R-CCTTCATTGGCTCATACCTC
SnRK2.5	F-CTACCGACTCAACTCACC	R-GTTCTCCGCTACACTTCT
SnRK2.6	F-CTTCCGCAAGACAATACA	R-AGATCAGATGACGGCACT
SnRK2.8	F-CCACAGATCACTCCGCCACC	R-TCGTCTTCGCTGAACCTCCC
SnRK2.9	F-TGCTCTTCCCGTCCAGTCAC	R-CCGGCCTTGCATATTCTCGT

Table 2 The primers for subcellular localization and overexpression analysis of FaPIN1

引物名称 Primer name	正向序列（5′-3′） Forward primer	反向序列（5′-3′） Reverse primer
PIN1-ORF	ATGATCACATTATCAGACTTTTAC	TCATAGCCCCAGCAAAATG
PIN1 for GFP	GAGAACACGGGGGACTCTAGAATGATCACATTATCAG ACTTTTAC	CGCCCTTGCTCACCATGGATCCTAGCCCCAGCAAA ATGTAG
PIN1 for pER8	CTAGTCGACTCTAGCCTCGAGATGATCACATTATCAGA CTTTTAC	GGGAGGCCTGGATCGACTAGTTCATAGCCCCAGCA AAATG

Fig. 1 The concentration effects of ABA inhibiting strawberry root growth（A）and the alleviation of exogenous ALA on the root growth of strawberry inhibited by ABA（B） The data in each figure are the means of more than 30 roots. The same small letters represent no significant difference. The same below.

Fig. 2 Effects of exogenous ABA and ALA on the endogenous IAA and ABA in the root-tips of strawberry

Fig. 3 Effects of ABA and ALA treatments on the gene expressions related to ABA signal in the root-tips of strawberry

Fig. 4 Effects of ABA and ALA treatments on the gene expressions related to IAA biosynthesis and transport in the root-tips of strawberry

Fig. 5 Effects of ALA and（or）ABA on auxin fluorescence signal intensity in the root tips of Arabidopsis A-C are PIN1，PIN2 and DR5 transgenic plants carried with green fluorescence protein gene（GFP）.The upper half is the fluorescence image，while the down half is the merged image with bright field. D is the relative fluorescence intensity of GFP related with IAA in three transgenic plants after treatments.

Fig. 6 Prediction of the transmembrane regions（A）and subcellular location（B）of FaPIN1 The blue rectangle indicates transmembrane domains located at either ends of the FaPIN1 protein in A.

Fig. 7 Phylogenetic analysis of FaPIN1

Fig. 8 Effect of ABA and ALA on root growth of FaPIN1 transgenic Arabidopsis

References 61

[1]	Akram N A, Ashraf M. 2013. Regulation in plant stress tolerance by a potential plant growth regulator,5-aminolevulinic acid. J Plant Growth Regul, 32 (3):663-679. doi: 10.1007/s00344-013-9325-9 URL
[2]	Ali B, Wang B, Ali S, Gill R A, Ali S, Rafiq M T, Xu L, Zhou W J. 2013. 5-Aminolevulinic acid ameliorates the growth,photosynthetic gas exchange capacity,and ultrastructural changes under cadmium stress in Brassica napus L. J Plant Growth Regul, 32 (3):604-614. doi: 10.1007/s00344-013-9328-6 URL
[3]	Ali B, Xu X, Gill R A, Yang S, Ali S, Tahir M, Zhou W J. 2014. Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crop Prod, 52:617-626. doi: 10.1016/j.indcrop.2013.11.033 URL
[4]	An Y Y, Cheng D X, Rao Z X, Sun Y P, Tang Q, Wang L J. 2019. 5-Aminolevulinic acid(ALA)promotes primary root elongation through modulation of auxin transport in Arabidopsis. Acta Physiol Plant, 41 (6):1-11. doi: 10.1007/s11738-018-2785-6
[5]	An Y Y, Liu L B, Chen L H, Sun Y P, Cao R, Wang L J. 2016a. ALA inhibits ABA-induced stomatal closure via reducing H₂O₂ and Ca²⁺ levels in guard cells. Front Plant Sci, 7:1-16.
[6]	An Y Y, Qi L, Wang L J. 2016b. ALA pretreatment improves waterlogging tolerance of fig plants. PLoS ONE, 11 (1):e0147202. doi: 10.1371/journal.pone.0147202 URL
[7]	An Y Y, Xiong L J, Hu S, Wang L J. 2020. PP2A and microtubules function in 5-aminolevulinic acid-mediated H₂O₂ signaling in Arabidopsis guard cells. Physiol Plant, 168 (3):709-724. doi: 10.1111/ppl.v168.3 URL
[8]	Antoni R, Rodriguez L, Gonzalez-Guzman M, Pizzio G A, Rodriguez P L. 2011. News on ABA transport,protein degradation,and ABFs/WRKYs in ABA signaling. Curr Opin Plant Biol, 14:547-553. doi: 10.1016/j.pbi.2011.06.004 URL
[9]	Baluška F, Mancuso S, Volkmann D, Barlow P W. 2010. Root apex transition zone:a signaling-response nexus in the root. Trends Plant Sci, 15 (7):402-408. doi: 10.1016/j.tplants.2010.04.007 URL
[10]	Belda-Palazón B, Adamo M, Valerio C, Ferreira L J, Confraria A, Reis-Barata D, Rodrigues A, Meyer C, Rodriguez P L, Baena-González. 2020. A dual function of SnRK 2 kinases in the regulation of SnRK1 and plant growth. Nat Plants, 6 (11):1345-1353. doi: 10.1038/s41477-020-00778-w pmid: 33077877
[11]	Bellini C, Pacurar D I, Perrone I. 2014. Adventitious roots and lateral roots:similarities and differences. Annu Rev Plant Biol, 65:639-666. doi: 10.1146/arplant.2014.65.issue-1 URL
[12]	Bindu R C, Vivekanandan M. 1998. Hormonal activities of 5-aminolevulinic acid in callus induction and micropropagation. Plant Growth Regul, 26 (1):15-18. doi: 10.1023/A:1006098005335 URL
[13]	Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B. 2007. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature, 433 (7021):39-44. doi: 10.1038/nature03184
[14]	Buer C S, Muday G K. 2004. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell, 16 (5):1191-1205. doi: 10.1105/tpc.020313 URL
[15]	Cai C Y, He S S, An Y Y, Wang L J. 2020. Exogenous 5-aminolevulinic acid improves strawberry tolerance to osmotic stress and its possible mechanisms. Physiol Plant, 168 (4):948-962. doi: 10.1111/ppl.13038 pmid: 31621913
[16]	Chandler P M, Robertson M. 1994. Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu Rev Plant Biol, 45 (1):113-141.
[17]	Chen Linghui, Liu Longbo, An Yuyan, Zhang Zhiping, Wang Liangju. 2014. Preliminary studies on the possible mechanism underlying 5-aminolevulinic acid-induced stomatal opening in apple leaves. Acta Horticulturae Sinica, 41 (10):1965-1974. (in Chinese)
	陈令会, 刘龙博, 安玉艳, 张治平, 汪良驹. 2014. 外源5-氨基乙酰丙酸促进苹果叶片气孔开放机理的初探. 园艺学报, 41 (10):1965-1974.
[18]	Cheng Y J, Guo W W, Yi H L, Pang X M, Deng X X. 2003. An efficient protocol for genomic DNA extraction from Citrus species. Plant Mol Biol Rep, 21 (2):177-178. doi: 10.1007/BF02774246 URL
[19]	Duan L, Dietrich D, Ng C H, Chan P M, Bhalerao R, Bennett M J, Dinneny J R. 2013. Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell, 25 (1):324-341. doi: 10.1105/tpc.112.107227 URL
[20]	Elansary H O, El-Ansary D O, Al-Mana F A. 2019. 5-Aminolevulinic acid and soil fertility enhance the resistance of rosemary to Alternaria dauci and Rhizoctonia solani and modulate plant biochemistry. Plants, 8 (12):585-610. doi: 10.3390/plants8120585 URL
[21]	Friml J. 2010. Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur J Cell Biol, 89 (2-3):231-235. doi: 10.1016/j.ejcb.2009.11.003 pmid: 19944476
[22]	Fu J J, Chu X T, Sun Y F, Miao Y J, Xu Y F, Hu T M. 2015. Nitric oxide mediates 5-aminolevulinic acid-induced antioxidant defense in leaves of Elymus nutans Griseb. exposed to chilling stress. PLoS ONE, 10 (7):e0130367. doi: 10.1371/journal.pone.0130367 URL
[23]	Fujii H, Verslues P E, Zhu J K. 2007. Identification of two protein kinases required for abscisic acid regulation of seed germination,root growth,and gene expression in Arabidopsis. Plant Cell, 19 (2):485-494. doi: 10.1105/tpc.106.048538 URL
[24]	Hotta Y, Tanaka T, Takaoka H, Takeuchi Y, Konnai M. 1997. New physiological effects of 5-aminolevulinic acid in plants:the increase of photosynthesis,chlorophyll content,and plant growth. Biosci Biotech Biochem, 61 (12):2025-2028. doi: 10.1271/bbb.61.2025 URL
[25]	Jaakola L, Pirttilä A M, Halonen M, Hohtola A. 2001. Isolation of high quality RNA from bilberry(Vaccinum myrtillus L.)fruit. Mol Biotechnol, 19 (2):201-203. doi: 10.1385/MB:19:2:201 pmid: 11725489
[26]	Kamiyama Y, Katagiri S, Umezawa T. 2021. Growth promotion or osmotic stress response:How SNF1-related protein kinase 2(SnRK2)kinases are activated and manage intracellular signaling in plants. Plants, 10 (7):1443-1461. doi: 10.3390/plants10071443 URL
[27]	Leung J, Giraudat J. 1998. Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol, 49 (1):199-222. doi: 10.1146/arplant.1998.49.issue-1 URL
[28]	Liu Longbo, An Yuyan, Xiong Lijun, Wang Liangju. 2016. Flavonols induced by 5-aminolevulinic acid are involved in regulation of stomatal opening in apple leaves. Acta Horticulturae Sinica, 43 (5):817-828. (in Chinese) doi: 10.16420/j.issn.0513-353x.2015-0873 URL
	刘龙博, 安玉艳, 熊丽君, 汪良驹. 2016. 5-ALA诱导的黄酮醇积累参与调节苹果叶片气孔开度. 园艺学报, 43 (5):817-828. doi: 10.16420/j.issn.0513-353x.2015-0873 URL
[29]	Lin Shaoyan, Zhang Fang, Xu Yingjie. 2016. The establishment of UPLC method for measuring polyamines content in plants. Journal of Nanjing Agricultural University, 39 (3):358-365. (in Chinese)
	林绍艳, 张芳, 徐颖洁. 2016. 植物中多胺含量超高效液相色谱法的建立. 南京农业大学学报, 39 (3):358-365.
[30]	Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-ΔΔCT method. Methods, 25 (4):402-408. doi: 10.1006/meth.2001.1262 pmid: 11846609
[31]	Mai C D, Phung N T, To H T, Gonin M, Hoang G T, Nguyen K L, Do V N, Courtois B, Gantet P. 2014. Genes controlling root development in rice. Rice, 7 (1):1-11. doi: 10.1186/1939-8433-7-1
[32]	Nishimura T, Matano N, Morishima T, Kakinuma C, Hayashi K, Komano T, Kubo M, Hasebe M, Kasahara H, Kamiya Y, Koshiba T. 2012. Identification of IAA transport inhibitors including compounds affecting cellular PIN trafficking by two chemical screening approaches using maize coleoptile systems. Plant Cell Physiol, 53 (10):1671-1682. doi: 10.1093/pcp/pcs112 pmid: 22875609
[33]	Pei Z M, Murata Y, Benning G, Thomine S, Klüsener B, Allen G J, Grill E, Schroeder J I. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature, 406 (6797):731-734. doi: 10.1038/35021067
[34]	Pilet P E, Chanson A. 1981. Effect of abscisic acid on maize root growth. A critical examination. Plant Sci Lett, 21 (2):99-106. doi: 10.1016/0304-4211(81)90175-9 URL
[35]	Promchuea S, Zhu Y, Chen Z, Jing Z, Gong Z. 2017. ARF 2 coordinates with PLETHORAs and PINs to orchestrate ABA-mediated root meristem activity in Arabidopsis. J Integr Plant Biol, 59 (1):30-43. doi: 10.1111/jipb.12506
[36]	Raheem A, Shaposhnikov A, Belimov A A, Dodd L C, Ali B. 2018. Auxin production by rhizobacteria was associated with improved yield of wheat(Triticum aestivum L.)under drought stress. Arch Agron Soil Sci, 64 (4):574-587. doi: 10.1080/03650340.2017.1362105 URL
[37]	Reddy K E, Lee W, Jeong J Y, Lee Y Y, Le H J, Kim M S, Kim D W, Yu D, Cho A, Oh Y K, Lee S D. 2018. Effects of deoxynivalenol-and zearalenone-contaminated feed on the gene expression profiles in the kidneys of piglets. Asian-Australas J Anim Sci, 31 (1):138-148. doi: 10.5713/ajas.17.0454 URL
[38]	Shen M, Zhang Z P, Wang L J. 2012. Effect of 5-aminolevulinic acid(ALA)on leaf diurnal photosynthetic characteristics and antioxidant activity in pear(Pyrus pyrifolia Nakai)//Mohammad M N. Applied photosynthesis. Intech:239-256.
[39]	Shi H, Zhu J K. 2002. Regulation of expression of the vacuolar Na⁺/H⁺ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol Biol, 50 (3):543-550. doi: 10.1023/A:1019859319617 URL
[40]	Slovak R, Ogura T, Satbhai S B, Ristova D, Busch W. 2015. Genetic control of root growth:from genes to networks. Ann Bot, 117 (1):9-24. doi: 10.1093/aob/mcv160 URL
[41]	Wang L, Hua D, He J, Duan Y, Chen Z, Hong X, Gong Z. 2011. Auxin response factor2(ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet, 7 (7):e1002172. doi: 10.1371/journal.pgen.1002172 URL
[42]	Wang L J, Jiang W B, Huang B J. 2004. Promotion of 5-aminolevulinic acid on photosynthesis of melon(Cucumis melo)seedlings under low light and chilling stress conditions. Physiol Plant, 121 (2):258-264. doi: 10.1111/ppl.2004.121.issue-2 URL
[43]	Wang L J, Jiang W B, Liu H, Liu W Q, Kang L, Hou X L. 2005. Promotion by 5-aminolevulinic acid of germination of pakchoi(Brassica campestris ssp. chinensis var. communis Tsen et Lee)seeds under salt stress. J Integr Plant Biol, 47 (9):1084-1091. doi: 10.1111/jipb.2005.47.issue-9 URL
[44]	Wang Liangju, Jiang Weibing, Zhang Zhen, Yao Quanhong, Matsui H, Ohara H. 2003. Biosynthesis and physiological activities of 5-aminolevulinic acid(ALA)and its potential application in agriculture. Plant Physiol Commu, 39 (3):185-192. (in Chinese)
	汪良驹, 姜卫兵, 章镇, 姚泉洪, 松井弘之, 小原均. 2003. 5-氨基乙酰丙酸的生物合成和生理活性及其在农业中的潜在应用. 植物生理学报, 39 (3):185-192.
[45]	Wang Liangju, Liu Weiqin, Sun Guorong, Wang Jianbo, Jiang Weibing, Liu Hui, Li Zhiqiang, Zhuang Meng. 2005. Effects of 5-aminolevulinic acid on photosynthesis and chlorophyll fluorescence of radish seedlings. Acta Bot Boreal-Occident Sin, 25 (3):488-496. (in Chinese)
	汪良驹, 刘卫琴, 孙国荣, 王建波, 姜卫兵, 刘晖, 李志强, 庄猛. 2005. ALA对萝卜不同叶位叶片光合作用与叶绿素荧光特性的影响. 西北植物学报, 25 (3):488-496.
[46]	Wang Liangju, Shi Wei, Liu Hui, Liu Weiqin, Jiang Weibing, Hou Xilin. 2004. Effects of exogenous 5-aminolevulinic acid treatment on leaf photosynthesis of pak-choi. J Nanjing Agric Univ, 27 (2):34-38. (in Chinese)
	汪良驹, 石伟, 刘晖, 刘卫琴, 姜卫兵, 侯喜林. 2004. 外源5-氨基乙酰丙酸处理对小白菜叶片的光合作用效应. 南京农业大学学报, 27 (2):34-38.
[47]	Wang P C, Zhao Y, Li Z, Hsu C C, Liu X, Fu L, Hou Y J, Du Y Y, Xie S J, Zhang C G, Gao J H, Cao M J, Huang X S, Zhu Y F, Tang K, Wang X, Tao W A, Xiong Y, Zhu J K. 2017. Reciprocal regulation of the tor kinase and ABA receptor balances plant growth and stress response. Mol Cell, 69 (1):100-112. doi: 10.1016/j.molcel.2017.12.002 URL
[48]	Wei Z, Li J. 2016. Brassinosteroids regulate root growth,development,and symbiosis. Mol Plant, 9 (1):86-100. doi: 10.1016/j.molp.2015.12.003 URL
[49]	Wei Z Y, Zhang Z P, Lee M R, Sun Y P, Wang L J. 2012. Effect of 5-aminolevulinic acid on leaf senescence and nitrogen metabolism of pakchoi under different nitrate levels. J Plant Nutr, 35 (1):49-63. doi: 10.1080/01904167.2012.631666 URL
[50]	Wu W W, He S S, An Y Y, Cao R X, Sun Y P, Tang Q, Wang L J. 2019a. Hydrogen peroxide as a mediator of 5-aminolevulinic acid-induced Na⁺ retention in roots for improving salt tolerance of strawberries. Physiol Plant, 167 (1):5-20.
[51]	Wu Wenwen, An Yuyan, Wang Liangju. 2017. Study on time effects of exogenous 5-aminolevulinic acid treatment on alleviating salinity injury in ‘Benihoppe’strawberry. Acta Horticulturae Sinica, 44 (6):1038-1048. (in Chinese) doi: 10.16420/j.issn.0513-353x.2017-0010
	吴雯雯, 安玉艳, 汪良驹. 2017. 5-氨基乙酰丙酸缓解‘红颜’草莓盐胁迫伤害的时间效应研究. 园艺学报, 44 (6):1038-1048. doi: 10.16420/j.issn.0513-353x.2017-0010
[52]	Wu Y, Liao W B, Dawuda M M, Hu L L, Yu J H. 2019b. 5-Aminolevulinic acid(ALA)biosynthetic and metabolic pathways and its role in higher plants:a review. Plant Growth Regul, 87:357-374. doi: 10.1007/s10725-018-0463-8
[53]	Xu L, Islam F, Zhang W F, Ghani M A, Ali B. 2018. 5-Aminolevulinic acid alleviates herbicide-induced physiological and ultrastructural changes in Brassica napus. J Integrat Agric, 17 (3):579-592.
[54]	Yang Guixiang, Peng Xianfeng, Zeng Zhenling, Cheng Zhangliu. 2005. Construction of expression vectors for detection of β estradiol. Sci Agric Sin,(5):1046-1051. (in Chinese)
	杨桂香, 彭险峰, 曾振灵, 陈杖榴. 2005. 雌二醇依赖性的细胞表达载体的研究. 中国农业科学,(5):1046-1051.
[55]	Yang H, Zhang J T, Zhang H W, Xu Y, An Y Y, Wang L J. 2021. Effect of 5-aminolevulinic acid(5-ALA)on leaf chlorophyll fast fluorescence characteristics and mineral element content of Buxus megistophylla grown along urban roadsides. Hortic, 7 (5):95-108. doi: 10.3390/horticulturae7050095 URL
[56]	Yuan Bingjian, Zhang Senlei, Cao Mengmeng, Wang Zhijuan, Li Xia. 2014. ABA modulates root growth through regulating auxin in Arabidopsis thaliana. Chin J Eco-Agric, 22 (11):1341-1347. (in Chinese)
	袁冰剑, 张森磊, 曹萌萌, 王志娟, 李霞. 2014. 脱落酸通过影响生长素合成及分布抑制拟南芥主根伸长. 中国生态农业学报, 22 (11):1341-1347.
[57]	Zhang H W, Tao H H, Yang H, Zhang L Z, Feng G Z, An Y Y, Wang L J. 2022. MdSCL 8 as a negative regulator participates in ALA-induced FLS1 to promote flavonol accumulation in apples. Int J Mol Sci, 23:2033-2048. doi: 10.3390/ijms23042033 URL
[58]	Zhang J, Davies W J. 1987. Increased synthesis of ABA in partially dehydrated root tips and ABA transport from roots to leaves. J Exp Bot, 38:2015-2023. doi: 10.1093/jxb/38.12.2015 URL
[59]	Zhao Y Y, Yan F, Hu L P, Zhou X T, Zou Z R, Cui L R. 2015. Effects of exogenous 5-aminolevulinic acid on photosynthesis,stomatal conductance,transpiration rate,and PIP gene expression of tomato seedlings subject to salinity stress. Genet Mol Res, 14 (2):6401-6412. doi: 10.4238/2015.June.11.16 pmid: 26125845
[60]	Zheng J, Liu L B, Tao H H, An Y Y, Wang L J. 2021. Transcriptomic profiling of apple calli with a focus on the key genes for ALA-induced anthocyanin accumulation. Front Plant Sci, 12:435.
[61]	Zuo J, Niu Q W, Møller S G, Chua N H. 2001. Chemical-regulated,site-specific DNA excision in transgenic plants. Nat Biotechnol, 19 (2):157-161. pmid: 11175731

Studies on Mechanisms of ALA Alleviating ABA Inhibiting Root Growth of Strawberry

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[1]	LIU Youxian, LI Guofang, TAN Ming, YANG Zhichang, ZHOU Shiwei, HUO Wenjing, ZHANG He, SUN Jianshe, and SHAO Jianzhu. Expression Analysis of MdTOPP13/28 During Axillary Bud Outgrowth in Malus [J]. Acta Horticulturae Sinica, 2023, 49(4): 697-712.
[2]	YU Tingting, LI Huan, NING Yuansheng, SONG Jianfei, PENG Lulin, JIA Junqi, ZHANG Weiwei, YANG Hongqiang. Genome-wide Identification of GRAS Gene Family in Apple and Expression Analysis of Its Response to Auxin [J]. Acta Horticulturae Sinica, 2023, 50(2): 397-409.
[3]	ZHENG Qingbo, BAO Zeyang, LAN Qingqing, ZHOU Yuwen, ZHOU Yufei, ZHENG Caixia, LI Xu. Advances in Studies on Adventitious Root Formation by Juvenile- and Auxin-determined [J]. Acta Horticulturae Sinica, 2023, 50(2): 441-450.
[4]	YUAN Xin, XU Yunhe, ZHANG Yupei, SHAN Nan, CHEN Chuying, WAN Chunpeng, KAI Wenbin, ZHAI Xiawan, CHEN Jinyin, GAN Zengyu. Studies on AcAREB1 Regulating the Expression of AcGH3.1 During Postharvest Ripening of Kiwifruit [J]. Acta Horticulturae Sinica, 2023, 50(1): 53-64.
[5]	ZHANG Xiaoming, YAN Guohua, ZHOU Yu, WANG Jing, DUAN Xuwei, WU Chuanbao, and ZHANG Kaichun. A New Sweet Cherry Rootstock Cultivar‘Jingchun 2’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 31-32.
[6]	YU Yangjun, WANG Weihong, SU Tongbing, ZHANG Fenglan, ZHANG Deshuang, ZHAO Xiuyun, YU Shuancang, LI Peirong, XIN Xiaoyun, and WANG Jiao. A New Chinese Cabbage Cultivar‘Jingchun CR3’with Clubroot Resistance and Bolting Tolerance [J]. Acta Horticulturae Sinica, 2022, 49(S2): 87-88.
[7]	WANG Lili, WANG Xin, WU Haidong, WEN Qiang, and Yang Xiaofei. A New Chinese Cabbage Cultivar‘Liaobai 28’with Resistance to Clubroot Disease [J]. Acta Horticulturae Sinica, 2022, 49(S2): 89-90.
[8]	TIAN Hongmei, LIU Juan, ZHANG Changkun, TAO Zhen, ZHANG Jian, and WANG Pengcheng, . A New Pumpkin Cultivar‘Wanzhen 6’for Melon Rootstock [J]. Acta Horticulturae Sinica, 2022, 49(S2): 127-128.
[9]	SUN Simiao, WANG Kun, GAO Yuan, WANG Dajiang, and LI Lianwen. A New Ornamental Crabapple Cultivar‘Zichen’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 267-268.
[10]	HU Ruolin, WANG Jiali, YANG Huiqin, YUAN Chao, NIU Yi, TANG Qinglin, WEI Dayong, TIAN Shibing, YANG Yang, WANG Zhimin. Cloning and Functional Analysis of Auxin Response Factor Gene SmARF5 in Solanum melongena [J]. Acta Horticulturae Sinica, 2022, 49(9): 1895-1906.
[11]	LIU Chaoyang, LIAO Zhichan, LU Xinxin, HE Yehua. Identification of CslD Gene Family in Pineapple and Functional Analysis of AcoCslD2a [J]. Acta Horticulturae Sinica, 2022, 49(8): 1650-1662.
[12]	WANG Yu, ZHANG Xue, ZHANG Xueying, ZHANG Siyu, WEN Tingting, WANG Yingjun, GAN Caixia, PANG Wenxing. The Effect of Camalexin on Chinese Cabbage Resistance to Clubroot [J]. Acta Horticulturae Sinica, 2022, 49(8): 1689-1698.
[13]	ZHANG Wanqing, ZHANG Hongxiao, LIAN Xiaofang, LI Yuying, GUO Lili, HOU Xiaogai. Analysis of DNA Methylation Related to Callus Differentiation and Rooting Induction of Paeonia ostii‘Fengdan’ [J]. Acta Horticulturae Sinica, 2022, 49(8): 1735-1746.
[14]	NIE Xinmiao, LUAN Heng, FENG Gaili, WANG Chao, LI Yan, WEI Min. Effects of Silicon Nutrition and Grafting Rootstocks on Chilling Tolerance of Cucumber Seedlings [J]. Acta Horticulturae Sinica, 2022, 49(8): 1795-1804.
[15]	ZHENG Xiaodong, XI Xiangli, LI Yuqi, SUN Zhijuan, MA Changqing, HAN Mingsan, LI Shaoxuan, TIAN Yike, WANG Caihong. Effects and Regulating Mechanism of Exogenous Brassinosteroids on the Growth of Malus hupehensis Under Saline-alkali Stress [J]. Acta Horticulturae Sinica, 2022, 49(7): 1401-1414.