Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Ultra-HPLC-MS pseudo-targeted metabolomic profiling reveals metabolites and associated metabolic pathway alterations in Asian plum (Prunus salicina) fruits in response to gummosis disease

Honghong Deng https://orcid.org/0000-0002-9036-8006 A * , Runmei He A , Hui Xia A , Nuo Xu A , Qunxian Deng A , Dong Liang A , Lijin Lin A , Ling Liao A , Bo Xiong https://orcid.org/0000-0002-1767-7478 A , Xinyu Xie A , Zhijian Gao A , Qingxuan Kang A and Zhihui Wang A *
+ Author Affiliations
- Author Affiliations

A Institute of Pomology and Olericulture, College of Horticulture, Sichuan Agricultural University, Chengdu 611130, China.


Handling Editor: Calum Wilson

Functional Plant Biology 49(11) 936-945 https://doi.org/10.1071/FP21168
Submitted: 2 June 2021  Accepted: 23 June 2022   Published: 12 July 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Plum (Prunus spp.) is an economically and nutritionally important stone fruit that is grown worldwide. Gummosis disease (GD) is one of the most common limiting factors that adversely affects the yield and quality of stone fruits such as plum. Elucidating plum fruit metabolomics responses is essential to develop sustainable agricultural practices to combat GD in the future. Herein, an ultra-high-performance liquid chromatography coupled to mass-spectrometry (UHPLC-MS) pseudo-targeted metabolomic profiling was first performed to elucidate the overall metabolic alterations in Asian plum (Prunus salicina Lindl.) fruit in response to GD. The most pivotal differential metabolites, including certain amino acids and proanthocyanidins, in GD and control groups were identified by combining multivariate data analysis with strict statistical criteria. Metabolic pathway enrichment analysis showed that GD induced a series of coordinated defence responses and reprogramming of various metabolic pathways, including glucosinolate biosynthesis, 2-oxocarboxylic acid metabolism, valine, leucine and isoleucine degradation, and isoquinoline alkaloid biosynthesis pathways. Using UHPLC-MS-based pseudo-targeted metabolomic profiling, we systematically evaluated overall metabolic modifications in Asian plum fruits in response to GD for the first time. The identified metabolic pathway alterations helped to better understand the internal relationships and related metabolic networks.

Keywords: Asian plum fruit, defense responses, gummosis disease, metabolic reprogramming, PCA, PLS-DA, pseudo-targeted metabolomic profiling, UHPLC-MS.


References

Alseekh S, Fernie AR (2018) Metabolomics 20 years on: what have we learned and what hurdles remain? The Plant Journal 94, 933–942.
Metabolomics 20 years on: what have we learned and what hurdles remain?Crossref | GoogleScholarGoogle Scholar | 29734513PubMed |

Batista-Silva W, Heinemann B, Rugen N, Nunes-Nesi A, Araújo WL, Braun HP, Hildebrandt TM (2019) The role of amino acid metabolism during abiotic stress release. Plant, Cell & Environment 42, 1630–1644.
The role of amino acid metabolism during abiotic stress release.Crossref | GoogleScholarGoogle Scholar |

Beckman TG, Pusey PL, Bertrand PF (2003) Impact of fungal gummosis on peach trees. HortScience 38, 1141–1143.
Impact of fungal gummosis on peach trees.Crossref | GoogleScholarGoogle Scholar |

Boothby D (1983) Gummosis of stone-fruit trees and their fruits. Journal of the Science of Food and Agriculture 34, 1–7.
Gummosis of stone-fruit trees and their fruits.Crossref | GoogleScholarGoogle Scholar |

Bowne JB, Erwin TA, Juttner J, Schnurbusch T, Langridge P, Bacic A, Roessner U (2012) Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Molecular Plant 5, 418–429.
Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level.Crossref | GoogleScholarGoogle Scholar | 22207720PubMed |

Burow M, Halkier BA, Kliebenstein DJ (2010) Regulatory networks of glucosinolates shape Arabidopsis thaliana fitness. Current Opinion in Plant Biology 13, 347–352.
Regulatory networks of glucosinolates shape Arabidopsis thaliana fitness.Crossref | GoogleScholarGoogle Scholar |

Cordell GA (2013) Fifty years of alkaloid biosynthesis in phytochemistry. Phytochemistry 91, 29–51.
Fifty years of alkaloid biosynthesis in phytochemistry.Crossref | GoogleScholarGoogle Scholar | 22721782PubMed |

Erb M (2018) Plant defenses against herbivory: closing the fitness gap. Trends in Plant Science 23, 187–194.
Plant defenses against herbivory: closing the fitness gap.Crossref | GoogleScholarGoogle Scholar | 29223923PubMed |

FAOSTAT (2018) Plums and sloes. Available at http://www.fao.org/faostat/en/#home

Gu L, Kelm MA, Hammerstone JF, Zhang Z, Beecher G, Holden J, Haytowitz D, Prior RL (2003) Liquid chromatographic/electrospray ionization mass spectrometric studies of proanthocyanidins in foods. Journal of Mass Spectrometry 38, 1272–1280.
Liquid chromatographic/electrospray ionization mass spectrometric studies of proanthocyanidins in foods.Crossref | GoogleScholarGoogle Scholar | 14696209PubMed |

Hellström JK, Törrönen AR, Mattila PH (2009) Proanthocyanidins in common food products of plant origin. Journal of Agricultural and Food Chemistry 57, 7899–7906.
Proanthocyanidins in common food products of plant origin.Crossref | GoogleScholarGoogle Scholar | 19722709PubMed |

Janick J (2005) The origins of fruits, fruit growing, and fruit breeding. In ‘Plant breeding reviews. Vol. 25’. (Ed. J Janick) pp. 255–320. (Wiley)
| Crossref |

Kalivodová A, Hron K, Filzmoser P, Najdekr L, Janečková H, Adam T (2015) PLS-DA for compositional data with application to metabolomics. Journal of Chemometrics 29, 21–28.
PLS-DA for compositional data with application to metabolomics.Crossref | GoogleScholarGoogle Scholar |

Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Research 34, D354–D357.
From genomics to chemical genomics: new developments in KEGG.Crossref | GoogleScholarGoogle Scholar | 16381885PubMed |

Khan N, Ali S, Shahid MA, Kharabian-Masouleh A (2017) Advances in detection of stress tolerance in plants through metabolomics approaches. Plant Omics Journal 10, 153–163.
Advances in detection of stress tolerance in plants through metabolomics approaches.Crossref | GoogleScholarGoogle Scholar |

Ko Y, Yao KS, Chen CY, Liu CW, Maruthasalam S, Lin CH (2008) First report of gummosis disease of plum (Prunus salicina) caused by a Botryosphaeria sp. in Taiwan. Plant Disease 92, 483
First report of gummosis disease of plum (Prunus salicina) caused by a Botryosphaeria sp. in Taiwan.Crossref | GoogleScholarGoogle Scholar | 30769694PubMed |

Kondo K, Kurihara M, Fukuhara K, Tanaka T, Suzuki T, Miyata N, Toyoda M (2000) Conversion of procyanidin B-type (catechin dimer) to A-type: evidence for abstraction of C-2 hydrogen in catechin during radical oxidation. Tetrahedron Letters 41, 485–488.
Conversion of procyanidin B-type (catechin dimer) to A-type: evidence for abstraction of C-2 hydrogen in catechin during radical oxidation.Crossref | GoogleScholarGoogle Scholar |

Matheron ME, Matejka JC (1992) Effects of temperature on sporulation and growth of Phytophthora citrophthora and P. parasitica and development of foot and root rot on citrus. Plant Disease 76, 1103–1109.
Effects of temperature on sporulation and growth of Phytophthora citrophthora and P. parasitica and development of foot and root rot on citrus.Crossref | GoogleScholarGoogle Scholar |

Mhlongo MI, Piater LA, Madala NE, Labuschagne N, Dubery IA (2018) The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Frontiers in Plant Science 9, 112
The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance.Crossref | GoogleScholarGoogle Scholar | 29479360PubMed |

Milosevic T, Milosevic N (2018) Plum (Prunus spp.) breeding. In ‘Advances in plant breed strategies: fruits’. 3rd edn. (Eds JM Al-Khayri, SM Jain, DV Johnson) pp. 165–215. (Springer International Publishing AG, part of Springer Nature: Cham, Switzerland)
| Crossref |

Munir S, Li Y, He P, He P, Ahmed A, Wu Y, He Y (2020) Unraveling the metabolite signature of citrus showing defense response towards Candidatus Liberibacter asiaticus after application of endophyte Bacillus subtilis L1-21. Microbiological Research 234, 126425
Unraveling the metabolite signature of citrus showing defense response towards Candidatus Liberibacter asiaticus after application of endophyte Bacillus subtilis L1-21.Crossref | GoogleScholarGoogle Scholar | 32035248PubMed |

Neilson EH, Goodger JQD, Woodrow IE, Møller BL (2013) Plant chemical defense: at what cost? Trends in Plant Science 18, 250–258.
Plant chemical defense: at what cost?Crossref | GoogleScholarGoogle Scholar | 23415056PubMed |

Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant Systematics and Evolution 266, 5–43.
Phylogeny and classification of Rosaceae.Crossref | GoogleScholarGoogle Scholar |

Rahman MA, Akond M, Babar MA, Beecher C, Erickson J, Thomason K, De Jong FA, Mason RE (2017) LC-HRMS based non-targeted metabolomic profiling of wheat (Triticum aestivum L.) under post-anthesis drought stress. American Journal of Plant Sciences 08, 3024–3061.
LC-HRMS based non-targeted metabolomic profiling of wheat (Triticum aestivum L.) under post-anthesis drought stress.Crossref | GoogleScholarGoogle Scholar |

Rauf A, Imran M, Abu-Izneid T Rauf A, Imran M, Abu-Izneid T Rauf A, Imran M, Abu-Izneid T (2019) Proanthocyanidins: a comprehensive review. Biomedicine & Pharmacotherapy 116, 108999
Proanthocyanidins: a comprehensive review.Crossref | GoogleScholarGoogle Scholar |

Ren S, Wang M (2014) General introduction of germplasm resources of Chinese plum and aprictot. In ‘Germplasm resources of Chinese plum and apricot’. (Eds R Shifu, W Min) pp. 16–31. (China Forestry Publishing House: Beijing) [In Chinese] Available at http://lycb.forestry.gov.cn

Rosik J, Kubala J, Kardosova A (1975) Amino acids and inorganic compounds in apricot tree gum (Prunus armeniaca L.) and in the polysaccharides prepared from this gum. Biologia (Bratisl) 30, 255–263.

Roussos PA, Efstathios N, Intidhar B, Denaxa NK, Tsafouros A (2016) Plum (Prunus domestica L. and P. salicina Lindl.). In ‘Nutritional composition of fruit cultivars’. (Eds M Simmonds, V Preedy) pp. 639–666. (Academic Press: London)
| Crossref |

Sharma JN, Gautam DR (1999) Gummosis complex in stone and nut fruits. In ‘Diseases of horticultural crop-fruits’. (Eds LR Verma, RC Sharma) pp. 275–290. (Indus Publishing Co.: New Delhi)

Siviero A, Cristofani M, Furtado EL, Garcia AAF, Coelho ASG, Machado MA (2006) Identification of QTLs associated with citrus resistance to Phytophthora gummosis. Journal of Applied Genetics 47, 23–28.
Identification of QTLs associated with citrus resistance to Phytophthora gummosis.Crossref | GoogleScholarGoogle Scholar | 16424605PubMed |

Sud M, Fahy E, Cotter D, Brown A, Dennis EA, Glass CK, Merrill AH, Murphy RC, Raetz CRH, Russell DW, Subramaniam S (2007) LMSD: LIPID MAPS structure database. Nucleic Acids Research 35, D527–D532.
LMSD: LIPID MAPS structure database.Crossref | GoogleScholarGoogle Scholar | 17098933PubMed |

Svoboda J, Boland W (2010) Plant defense elicitors: analogues of jasmonoyl–isoleucine conjugate. Phytochemistry 71, 1445–1449.
Plant defense elicitors: analogues of jasmonoyl–isoleucine conjugate.Crossref | GoogleScholarGoogle Scholar | 20570297PubMed |

Traka MH (2016) Health benefits of glucosinolates. In ‘Advaces in botanical research’. (Ed. S Kopriva) pp. 247–279. (Academic Press: London)
| Crossref |

Variyar PS, Banerjee A, Akkarakaran JJ, Suprasanna P (2014) Role of glucosinolates in plant stress tolerance. In ‘Emerging technologies and management of crop stress tolerance: biological techniques’. (Eds P Ahmad, S Rasool) pp. 271–291. (Academic Press: London)
| Crossref |

Wen B, Mei Z, Zeng C, Liu S (2017) metaX: a flexible and comprehensive software for processing metabolomics data. BMC Bioinformatics 18, 183
metaX: a flexible and comprehensive software for processing metabolomics data.Crossref | GoogleScholarGoogle Scholar | 28327092PubMed |

Weaver DJ (1974) A gummosis disease of peach trees caused by Botryosphaeria dothidea. Phytopathology 64, 1429–1432.
A gummosis disease of peach trees caused by Botryosphaeria dothidea.Crossref | GoogleScholarGoogle Scholar |

Wishart DS, Feunang YD, Marcu A, Guo AC, Liang K, Vázquez-Fresno R, Sajed T, Johnson D, Li C, Karu N, Sayeeda Z, Lo E, Assempour N, Berjanskii M, Singhal S, Arndt D, Liang Y, Badran H, Grant J, Serra-Cayuela A, Liu Y, Mandal R, Neveu V, Pon A, Knox C, Wilson M, Manach C, Scalbert A (2018) HMDB 4.0: the human metabolome database for 2018. Nucleic Acids Research 46, D608–D617.
HMDB 4.0: the human metabolome database for 2018.Crossref | GoogleScholarGoogle Scholar | 29140435PubMed |

Worley B, Powers R (2013) Multivariate analysis in metabolomics. Current Metabolomics 1, 92–107.
Multivariate analysis in metabolomics.Crossref | GoogleScholarGoogle Scholar | 26078916PubMed |

Xu J, Li J, Zhang R, He J, Chen Y, Bi N, Song Y, Wang L, Zhan Q, Abliz Z (2019) Development of a metabolic pathway-based pseudo-targeted metabolomics method using liquid chromatography coupled with mass spectrometry. Talanta 192, 160–168.
Development of a metabolic pathway-based pseudo-targeted metabolomics method using liquid chromatography coupled with mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 30348373PubMed |

Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant, Cell & Environment 36, 2085–2103.
New insights into the regulation of plant immunity by amino acid metabolic pathways.Crossref | GoogleScholarGoogle Scholar |