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Comparative analysis of transcriptomic profiling to identify genes involved in the bulged surface of pear fruit (Pyrus bretschneideri Rehd. cv. Yuluxiangli)

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Abstract

Pear (Pyrus spp.) belongs to the genus Pyrus, in the family Rosaceae. Some varieties of pear fruit exhibit bulged surface, which seriously affects the quality and commodity value of the pear fruit. In this study, we performed anatomical, physiological, and transcriptomic analysis to explore the mechanism of paclobutrazol (PBZ) on the bulged surface of pear fruit. The vascular bundles of flesh were more evenly distributed, and the fruit cells were more compactly arranged and smaller in size treated with PBZ. However, the auxin (IAA) content of flesh was decreased in the treated group. Furthermore, the GO and KEGG analysis of differentially expressed genes (DEGs) showed that auxin, phenylpropanoid metabolic pathways, and transcriptional factor genes were significantly enriched on the relieved bulged surface of pear fruit. And it was analyzed that some genes contained auxin responded cis-elements from the selected DEGs in the promoter region. We conclude that PBZ plays a negative role in cell division, cell elongation, and vascular bundle development on the bulged surface of pear fruit through the involvement of auxin-related genes. This study will provide a theoretical basis for the regulation of the bulged surface of pear fruit by a growth retardant agent.

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Availability of data and materials

The datasets used and analyzed during the above research are available from the Additional file or corresponding author. The pear genome datasets used during the current study are available on the website(http://gigadb.org). The RNA-seq data were deposited in the NCBI bio project (https://www.ncbi.nlm.nih.gov/bioproject/) under accession number PRJNA627328.

Abbreviations

IAA:

Auxin

GH3:

Gretchen hagen3

KEGG:

Kyoto Encyclopedia of Genes and Genomes

PBZ:

Paclobutrazol

PK:

Paclobutrazol treatment

CK:

DdH2O treatment

DEGs:

Differentially expressed genes

PIN:

Pin-formed 1

AUX:

Auxin influx carrier

COMT:

Caffeic acid 3-O-methyltransferase

4CL:

4-Coumarate-CoA ligase 1

CYP73A2:

Cytochrome P450 73A2

CSE:

Caffeoyl shikimate esterase

NAC:

Domain-containing protein 2

DOF4.6:

Dof zinc finger protein

CesA:

Cellulose synthase A

References

  • Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Plants 19:307–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arreewichit P, Sae-Lim P, Nirapathpongporn K, Viboonjun U, Kongsawadworakul P, Narangajavana J (2019) Opposite physiological effects upon jasmonic acid and brassinosteroid treatment on laticifer proliferation and co-occurrence of differential expression of genes involved in vascular development in rubber tree. Physiol Mol Biol Plants 25:1283–1299

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bell-Lelong DA, Cusumano JC, Meyer K, Chapple C (1997) Cinnamate-4-hydroxylase expression in Arabidopsis. Regulation in response to development and the environment. Plant Physiol 13:729–738

    Google Scholar 

  • Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    CAS  PubMed  Google Scholar 

  • Bruck DK, Paolillo DJ (1984) Replacement of leaf primordia with IAA in the induction of vascular differentiation in the stem of colecus. New Phytol 96:353–370

    Google Scholar 

  • Burondkar MM, Upreti KK, Ambavane AR, Rajan S, Mahadik SG, Bhave SG (2016) Hormonal changes during flowering in response to paclobutrazol application in mango cv. Alphonso under konkan conditions. Indian J Plant Physiol 21:306–311

    Google Scholar 

  • Cao Y, Meng D, Han Y, Chen T, Jiao C, Chen Y, Jin Q, Cai Y (2019) Comparative analysis of B-BOX genes and their expression pattern analysis under various treatments in Dendrobium officinale. BMC Plant Biol 19:245

    PubMed  PubMed Central  Google Scholar 

  • Chen FY, Ni HZ, Wang Y, Ren ZC (2011) Effect of paclobutrazol (PP_333) on growth and fruiting of Dongkui bayberry(Myrica rubra). Asian J Ecotoxicol 6:661–666

    CAS  Google Scholar 

  • Chen J (2009) Effects of growth regulant on development of calyx and dynamic change of endogenous hormone and fruit quality in Chinese pear ‘Dangshansuli’. Anhui Agric Univ

  • Chen YY, Li K, Song YQ, Li N, Li LL (2018) Effect of growth regulator PBO on fruit decalyx and quality of pear. South China Fruits 47:55–58

    Google Scholar 

  • De Rybel B, Möller B, Yoshida S, Grabowicz I, Barbier de Reuille P, Boeren S, Smith RS, Borst JW, Weijers DA (2013) bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev Cell 24:426–437

    PubMed  Google Scholar 

  • Dhonukshe D, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17:520–527

    CAS  PubMed  Google Scholar 

  • Fang ZG, Zhao XF (2005) Effects of paclobutrazol (PP333) on free endogenous hormones concentration in the leaves of rice and wheat seedling. J Laiyang Agric Col 22:101–104

    Google Scholar 

  • Friml J (2003) Auxin transport-shaping the plant. Curr Opin Plant Biol 6:7–12

    CAS  PubMed  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 28:2226–2230

    Google Scholar 

  • Gören-Sağlam N, Harrison E, Breeze E, Öz G, Buchanan-Wollaston V (2020) Analysis of the impact of indole-3-acetic acid (IAA) on gene expression during leaf senescence in Arabidopsis thaliana. Physiol Mol Biol Plants 26:733–745

    PubMed  PubMed Central  Google Scholar 

  • Groover AT, Pattishall A, Jones AM (2003) IAA 8 expression during vascular cell differentiation. Plant Mol Biol 51:427–435

    CAS  PubMed  Google Scholar 

  • Hao GW, Bai MD, Gao P, Yang S, Guo HP (2016) Effect of growth regulator on decalyx rate and fruit quality of pear. Shanxi Fruits 5:15–18

    CAS  Google Scholar 

  • Hu WJ, Kawaoka A, Tsai CJ, Lung J, Osakabe K, Ebinuma H, Chiang VL (1998) Compartmentalized expression of two structurally and functionally distinct 4-coumarate: CoA ligase genes in aspen (Populus tremuloides). Proc Natl Acad Sci USA 95:5407–5412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katayama H, Iwamoto K, Kariya Y, Asakawa T, Kan T, Fukuda H, Ohashi-Ito KA (2015) A negative feedback loop controlling bHLH complexes is involved in vascular cell division and differentiation in the root apical meristem. Curr Biol:CB 25:3144–3150

    CAS  PubMed  Google Scholar 

  • Koukourikou-Petridou MA (1996) Paclobutrazol affects the extension growth and the levels of endogenous IAA of almond seedlings. Plant Growth Regul 18:187–190

    CAS  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantC ARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin CY, Wang JP, Li Q, Chen HC, Liu J, Loziuk P, Song J, Williams C, Muddiman DC, Sederoff RR, Chiang VL (2015) 4-coumaroyl and caffeoyl shikimic acids inhibit 4-coumaric acid: coenzyme a ligases and modulate metabolic flux for 3-hydroxylation in monolignol biosynthesis of Populus trichocarpa. Mol Plant 8:176–187

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△Ct method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma CL, Chen SY, Liu XH (2000) Effects of PP 333 on tissue structure in leaves, cold resistance and growth of shoots of pummelo trees. Fujian J Agric Sci 15:26–29

    Google Scholar 

  • Ma HC, Wang YL, Wen X, Qi M, Li J (2011) Effects of different reagent treatments on the microstructure of calyx tube with or without calyx of Korla fragrant pear. J Fruit Sci 28:518–520+551.

  • Ma HY, Tao ST, Chen Y, Yu RR, Chen XY, Bao JP, Wu CY, Zhang R (2019) Study on relationship between vascular bundle and sepal abscission in different orders of inflorescenceson short fruiting branches of Korla fragrant pear. Acta Agric Jiangxi 31:26–30

    Google Scholar 

  • Ma XH (1996) Making transparent vascular bundle skillfully by dyeing. Bul Biol 31:14

    Google Scholar 

  • Ma YL, Steeves TA (1992) Auxin effects on vascular differentiation in ostrich fern. Ann Bot 70:277–282

    CAS  Google Scholar 

  • Mittag J, Šola I, Rusak G, Ludwig-Müller J (2015) Physcomitrella patens auxin conjugate synthetase (GH3) double knockout mutants are more resistant to Pythium infection than wild type. J Plant Physiol 183:75–83

    CAS  PubMed  Google Scholar 

  • Moreno-Piovano GS, Moreno JE, Cabello JV, Arce AL, Otegui ME, Chan RL (2017) A role for LAX2 in regulating xylem development and lateral-vein symmetry in the leaf. Ann Bot 120:577–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nairn CJ, Haselkorn T (2005) Three loblolly pine CesA genes expressed in developing xylem are orthologous to secondary cell wall CesA genes of angiosperms. New Phytol 166:907–915

    CAS  PubMed  Google Scholar 

  • Nii N (1980) Seasonal changes in growth and enlargement of the Japanese fruit, Pyrus Serotina cv Shinseiki, in relation to vascular bundle development in the pedicel and flesh. J Hort Sci 55:385–396

    Google Scholar 

  • Ohashi-Ito K, Fukuda H (2016) Functional mechanism of bHLH complexes during early vascular development. Curr Opin Plant Biol 33:42–47

    CAS  PubMed  Google Scholar 

  • Ohashi-Ito K, Oda Y, Fukuda H (2010) Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22:3461–3473

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohashi-ito K, Oguchi M, Kojima M, Sakakibara H, Fukuda H (2013) Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY. Development 140:765–769

    CAS  PubMed  Google Scholar 

  • Péret B, Swarup K, Ferguson A, Seth M, Yang YD et al (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24:2874–2885

    PubMed  PubMed Central  Google Scholar 

  • Qi HY, Li T, Liu HT, Zhang J (2006) Change in 14 C-soluble sugar involved in the photosynthate translocation pathway of tomato. Agric Sci China 5:209–215

    CAS  Google Scholar 

  • Qi XX, Wu J, Wang LF, Li LT, Cao YF, Tian LM, Dong XG, Zhang SL (2013) Identifying the candidate genes involved in the calyx abscission process of ‘kuerlexiangli’ (Pyrus Sinkiangensis Yu) by digital transcript abundance measurements. BMC Genomics 14:727–739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qin GX, Zhang GQ, Zhai QX, Zhang Y, Wang YJ (2004) Effect of PP333 on the cell anatomy structure of the secondary xylem of greenhouse cultivated grape. J Fruit Sci 21:480–481

    Google Scholar 

  • Renée G, Roger P, Dubacq JP (1983) situ and IAA-induced cell elongation is correlated to the oleyl phos-phatidylcholine content along the vigna radiata hypocotyl. Plant Cell Physiol 24:541–549

    Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Gene Dev 20:1015–1027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su L, Bassa C, Audran C, Mila I, Cheniclet C, Chevalier C, Bouzayen M, Roustan J, Chervin C (2014) The auxin Sl-IAA17 transcriptional repressor controls fruit size via the regulation of endoreduplication-related cell expansion. Plant Cell Physiol 55:1969–1976

    CAS  PubMed  Google Scholar 

  • Teng YW (2017) Advances in the research on phylogeny of the genus Pyrus and the origin of pear cultivars native to East Asia. J Fruit Sci 34:370–378

    Google Scholar 

  • Weng JK, Mo H, Chapple C (2010) Over-expression of F5H in COMT-deficient Arabidopsis leads to enrichment of an unusual lignin and disruption of pollen wall formation. Plant J 64:898–911

    CAS  PubMed  Google Scholar 

  • Wenzel CL, Schuetz M, Yu Q, Mattsson J (2010) Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49:387–398

    Google Scholar 

  • Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883–883

    PubMed  Google Scholar 

  • Wu J, Wang YT, Xu JB, Korban SS, Fei ZJ et al (2018) Diversification and independent domestication of Asian and European pears. Genome Biol 19:77

    PubMed  PubMed Central  Google Scholar 

  • Xie ZS, Cao HM, Liu AL, Wang B, Wang SP (2011) The effects of root restriction on water transport in the vascular bundle of grape fruit during different stages of development. Plant Physiol J 47:899–903

    Google Scholar 

  • Xue GX, Wu XY, Wang Y, Fan LQ (1999) Effect of GA and PP333 on longitudinal diametre and diametre of apple-pear. J Agric Sci Yanbian Univ 2:95–97

    Google Scholar 

  • Yamaguchi M, Goué N, Igarashi H, Ohtani M, Nakano Y et al (2010a) VASCULAR-RELATED NAC-DOMAIN 6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 153:906–914

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi M, Mitsuda N, Ohtani M, Ohme-takagi M, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 66:579–590

    CAS  PubMed  Google Scholar 

  • Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T (2010b) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22:1249–1263

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Chen F, Yu O, Beachy RN (2010) Controlled silencing of 4-coumarate:CoA ligase alters lignocellulose composition without affecting stem growth. Plant Physiol Biochem 49:103–109

    PubMed  Google Scholar 

  • Yang L, Qin ZQ, Wu T, Li XM, Tu JF, Yang FC, Zhu HY, Liu Z (2017) Paraffin section preparation of pear fresh tissue at different development stages. Bul Agril Sci Tech 12:213–215

    Google Scholar 

  • Yao Q, Zhu HH, Chen JZ (2005) Growth responses and endogenous IAA and iPAs changes of litchi (Litchi chinensis Sonn.) seedlings induced by arbuscular mycorrhizal fungal inoculation. Sci Hortic 105:145–151

    CAS  Google Scholar 

  • Zhang X, Zhang LJ, Zhang QP, Xu JY, Liu WS, Dong WX (2017) Comparative transcriptome profiling and morphology provide insights into endocarp cleaving of apricot cultivar (Prunus armeniaca L.). BMC Plant Biol 17:72

    PubMed  PubMed Central  Google Scholar 

  • Zhang YX, Han XJ, Sang J, He XL, Liu MY, Qiao GR, Zhuo RY, He GP, Hu JJ (2016) Transcriptome analysis of immature xylem in the Chinese fir at different developmental phases. Peer J 4:e2097

    PubMed  PubMed Central  Google Scholar 

  • Zhang ZY, Li JJ, Tang ZS, Sun XM, Zhang HL et al (2018) Gnp4/LAX2, a RAWUL protein, interferes with the OsIAA3-OsARF25 interaction to regulate grain length via the auxin signaling pathway in rice. J Exp Bot 69:4723–4737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong RQ, Morrison H, Freshour GD, Hahn MG, Ye ZH (2003) Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative effect on cellulose biosynthesis. Plant Physiol 132:786–795

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong RQ, Ye ZH (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53:368–380

    CAS  PubMed  Google Scholar 

  • Zhong RQ, Ye ZH (2014) Complexity of the transcriptional network controlling secondary wall biosynthesis. Plant Sci 229:193–207

    CAS  PubMed  Google Scholar 

  • Zhou WQ, Yang WL, Zhao SL, Man SE, Na SE, Qi YQ, Liao K (2017) Response of leaf tissue structure to PP333 in Korla fragrant pear. Agric Sci Technol 18:1805-1807+1815

    Google Scholar 

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Funding

This work was supported in part by grants from the National Key R&D Program of China (2018YFD0201407), Excellent Ph.D. Reward Project Fund of Shanxi Province (SXYBKY201736), and Key Research and Development (Agriculture) Program of Shanxi Province (201703D211011-2). These fundings provided the financial support to the research projects but did not contain project design, data collection, analysis, or preparation of the manuscript.

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Authors and Affiliations

  1. College of Forestry, Shanxi Agricultural University, Taigu, 030801, Shanxi, China

    Baopeng Ding & Youzhi Han

  2. College of Horticulture, Shanxi Agricultural University, Taigu, 030801, Shanxi, China

    Baopeng Ding, Tingting Liu, Chaohui Hu, Yuqin Song, Ruijie Hao, Xinxin Feng, Tingting Cui & Liulin Li

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  1. Baopeng Ding
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  2. Tingting Liu
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  3. Chaohui Hu
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Contributions

LL planned and designed the research.YH guided and supported this research. BD collected the plant materials, performed the experiment, analyzed the data, interpreted results, and wrote the manuscript.TL revisied the language and checked the exprimental data. CH and TC contributed to sample data collection. YS analyzed the part of data. RH and XF provided suggestions in drafting the manuscript and edited the manuscript. All the authors have read and approved the final manuscript.

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Correspondence to Youzhi Han or Liulin Li.

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Additional file 1

: Fig. S1. Graph of the bulged surface of pear fruit at the different development stages.The bulged surface of pear fruit at the early, middle and late stage of fruit.

Additional file 2

: Fig. S2. Differentially expressed vol diagram. The Y-axis shows the log2 FPKM values, FPKM (Fragments Per Kilobase of exon model per Million mapped reads) values, X-axis shows log2 fold change. Red, green and black indicate up, down and unchanged expression, respectively (Fold change≥1,p-value<0.05).

Additional file 3

: Table S1. Statistics of differentially expressed genes in response to PBZ.

Additional file 4

: Table S2. The number of differential expressions annotated genes in the database.

Additional file 5

: Table S3. The list of differentially expressed genes.

Additional file 6

: Table S4. The list genes of GO enrichment.

Additional file 7

: Table S5. The list of genes enriched on the KEGG pathway.

Additional file 8

: Table S6. Identification genes involved in the bulged surface of pear fruit.

Additional file 9

: Table S7 Primers used to perform qRT-PCR of selected candidate genes.

Additional file 10

: Table S8. Quantitative RT-PCR method.

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Ding, B., Liu, T., Hu, C. et al. Comparative analysis of transcriptomic profiling to identify genes involved in the bulged surface of pear fruit (Pyrus bretschneideri Rehd. cv. Yuluxiangli). Physiol Mol Biol Plants 27, 69–80 (2021). https://doi.org/10.1007/s12298-021-00929-z

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