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Knockdown of CaHSP60-6 confers enhanced sensitivity to heat stress in pepper (Capsicum annuum L.)

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Abstract

Main conclusion

HSP60 gene family in pepper was analyzed through bioinformatics along with transcriptional regulation against multiple abiotic and hormonal stresses. Furthermore, the knockdown of CaHSP60-6 increased sensitivity to heat stress.

Abstract

The 60 kDa heat shock protein (HSP60) also known as chaperonin (cpn60) is encoded by multi-gene family that plays an important role in plant growth, development and in stress response as a molecular chaperone. However, little is known about the HSP60 gene family in pepper (Capsicum annuum L.). In this study, 16 putative pepper HSP60 genes were identified through bioinformatic tools. The phylogenetic tree revealed that eight of the pepper HSP60 genes (50%) clustered into group I, three (19%) into group II, and five (31%) into group III. Twelve (75%) CaHSP60 genes have more than 10 introns, while only a single gene contained no introns. Chromosomal mapping revealed that the tandem and segmental duplication events occurred in the process of evolution. Gene ontology enrichment analysis predicted that CaHSP60 genes were responsible for protein folding and refolding in an ATP-dependent manner in response to various stresses in the biological processes category. Multiple stress-related cis-regulatory elements were found in the promoter region of these CaHSP60 genes, which indicated that these genes were regulated in response to multiple stresses. Tissue-specific expression was studied under normal conditions and induced under 2 h of heat stress measured by RNA-Seq data and qRT-PCR in different tissues (roots, stems, leaves, and flowers). The data implied that HSP60 genes play a crucial role in pepper growth, development, and stress responses. Fifteen (93%) CaHSP60 genes were induced in both, thermo-sensitive B6 and thermo-tolerant R9 lines under heat treatment. The relative expression of nine representative CaHSP60 genes in response to other abiotic stresses (cold, NaCl, and mannitol) and hormonal applications [ABA, methyl jasmonate (MeJA), and salicylic acid (SA)] was also evaluated. Knockdown of CaHSP60-6 increased the sensitivity to heat shock treatment as documented by a higher relative electrolyte leakage, lipid peroxidation, and reactive oxygen species accumulation in silenced pepper plants along with a substantial lower chlorophyll content and antioxidant enzyme activity. These results suggested that HSP60 might act as a positive regulator in pepper defense against heat and other abiotic stresses. Our results provide a basis for further functional analysis of HSP60 genes in pepper.

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Abbreviations

DAB:

Diaminobenzidine

HS:

Heat stress

HSP:

Heat shock protein

MeJA:

Methyl jasmonate

NBT:

Nitro-blue tetrazolium

PDS:

Phytoene desaturase

ROS:

Reactive oxygen species

SA:

Salicylic acid

TRV:

Tobacco rattle virus

VIGS:

Virus-induced gene silencing

References

  • Ahuja I, de Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    CAS  PubMed  Google Scholar 

  • Alam MN, Zhang L, Yang L et al (2018) Transcriptomic profiling of tall fescue in response to heat stress and improved thermotolerance by melatonin and 24-epibrassinolide. BMC Genom 19:224. https://doi.org/10.1186/s12864-018-4588

    Article  Google Scholar 

  • Ali M, Luo D-X, Khan A et al (2018) Classification and genome-wide analysis of chitin-binding proteins gene family in pepper (Capsicum annuum L.) and transcriptional regulation to phytophthora capsici, abiotic stresses and hormonal applications. Int J Mol Sci 19:2216. https://doi.org/10.3390/ijms19082216

    Article  CAS  PubMed Central  Google Scholar 

  • Ali M, Gai W-X, Khattak AM et al (2019) Knockdown of the chitin-binding protein family gene CaChiIV1 increased sensitivity to Phytophthora capsici and drought stress in pepper plants. Mol Genet Genom. https://doi.org/10.1007/s00438-019-01583-7

    Article  Google Scholar 

  • Al-whaibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ Sci 23:139–150. https://doi.org/10.1016/j.jksus.2010.06.022

    Article  Google Scholar 

  • Augustine SM, Cherian AV, Syamaladevi DP, Subramonian N (2015) Erianthus arundinaceus HSP70 (EaHSP70) acts as a key regulator in the formation of anisotropic interdigitation in sugarcane (Saccharum spp. hybrid) in response to drought stress. Plant Cell Physiol 56:2368–2380

    CAS  PubMed  Google Scholar 

  • Balbuena TS, Salas JJ, Martínez-Force E et al (2011) Proteome analysis of cold acclimation in sunflower. J Proteome Res 10:2330–2346

    CAS  PubMed  Google Scholar 

  • Balchin D, Hayer-Hartl M, Hartl FU (2016) In vivo aspects of protein folding and quality control. Science 353:aac4354. https://doi.org/10.1126/science.aac4354

    Article  CAS  PubMed  Google Scholar 

  • Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292. https://doi.org/10.1078/0176-1617-00833

    Article  CAS  PubMed  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A et al (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    PubMed  PubMed Central  Google Scholar 

  • Cheng L, Zou Y, Ding S et al (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499

    CAS  PubMed  Google Scholar 

  • Cho EK, Hong CB (2006) Over-expression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. Plant Cell Rep 25:349–358. https://doi.org/10.1007/s00299-005-0093-2

    Article  CAS  PubMed  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867. https://doi.org/10.1111/tpj.13299

    Article  CAS  PubMed  Google Scholar 

  • Dai Y, Shen Z, Liu Y et al (2009) Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot 65:177–182. https://doi.org/10.1016/j.envexpbot.2008.12.008

    Article  CAS  Google Scholar 

  • Deng W, Wang Y, Liu Z et al (2014) HemI: a toolkit for illustrating heatmaps. PLoS One 9:e111988. https://doi.org/10.1371/journal.pone.0111988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duck N, McCormick S, Winter J (1989) Heat shock protein 70 cognate expression in vegetative and reproductive organs of Lycopersicon esculentum. Proc Natl Acad Sci USA 86:3674–3678

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fan F, Kang Y, Yang X et al (2017) The DnaJ gene family in pepper (Capsicum annuum L.): comprehensive identification, characterization and expression profiles. Front Plant Sci 8:1–11. https://doi.org/10.3389/fpls.2017.00689

    Article  Google Scholar 

  • Feng X, Zhang H, Ali M et al (2019) A small heat shock protein CaHsp25.9 positively regulates heat, salt, and drought stress tolerance in pepper (Capsicum annuum L.). Plant Physiol Biochem 142:151–162. https://doi.org/10.1016/j.plaphy.2019.07.001

    Article  CAS  PubMed  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C et al (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gu Z, Cavalcanti A, Chen F-C et al (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262

    CAS  PubMed  Google Scholar 

  • Guo WL, Chen RG, Gong ZH et al (2012) Exogenous abscisic acid increases antioxidant enzymes and related gene expression in pepper (Capsicum annuum) leaves subjected to chilling stress. Genet Mol Res 11:4063–4080

    CAS  PubMed  Google Scholar 

  • Guo M, Liu J-H, Lu J-P et al (2015) Genome-wide analysis of the CaHsp20 gene family in pepper: comprehensive sequence and expression profile analysis under heat stress. Front Plant Sci 6:806

    PubMed  PubMed Central  Google Scholar 

  • Guo M, Liu JH, Ma X et al (2016) Genome-wide analysis of the Hsp70 family genes in pepper (Capsicum annuum L.) and functional identification of CaHsp70-2 involvement in heat stress. Plant Sci 252:246–256. https://doi.org/10.1016/j.plantsci.2016.07.001

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular c haperones in protein folding and proteostasis. Nature 475:324–332. https://doi.org/10.1038/nature10317

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Park K-J, Obayashi T et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    PubMed  PubMed Central  Google Scholar 

  • Huang L, Cheng G, Khan A et al (2018) CaHSP16.4, a small heat shock protein gene in pepper, is involved in heat and drought tolerance. Protoplasma 256:39. https://doi.org/10.1007/s00709-018-1280-7

    Article  CAS  PubMed  Google Scholar 

  • Ishida R, Okamoto T, Motojima F et al (2018) Physicochemical properties of the mammalian molecular chaperone HSP60. Int J Mol Sci 19:e489. https://doi.org/10.3390/ijms19020489

    Article  CAS  PubMed  Google Scholar 

  • Jungkunz I, Link K, Vogel F et al (2011) AtHsp70-15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. Plant J 66:983–995

    CAS  PubMed  Google Scholar 

  • Kang W-H, Kim S, Lee H-A et al (2016) Genome-wide analysis of Dof transcription factors reveals functional characteristics during development and response to biotic stresses in pepper. Sci Rep 6:33332

    PubMed  PubMed Central  Google Scholar 

  • Khan A, Li R-J, Sun J-T et al (2018) Genome-wide analysis of dirigent gene family in pepper (Capsicum annuum L.) and characterization of CaDIR7 in biotic and abiotic stresses. Sci Rep 8:5500. https://doi.org/10.1038/s41598-018-23761-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H-J, Hwang NR, Lee K-J (2007) Heat shock responses for understanding diseases of protein denaturation. Mol Cells (Springer Sci Bus Media BV) 23:123–131

    Google Scholar 

  • Kim S, Park M, Yeom SI et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum sp. Nat Genet 46:270–278. https://doi.org/10.1038/ng.2877

    Article  CAS  PubMed  Google Scholar 

  • Komatsu S, Yamamoto A, Nakamura T et al (2011) Comprehensive analysis of mitochondria in roots and hypocotyls of soybean under flooding stress using proteomics and metabolomics techniques. J Proteome Res 10:3993–4004

    CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U et al (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    CAS  PubMed  Google Scholar 

  • Lavania D, Dhingra A, Siddiqui MH et al (2015) Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant Physiol Biochem 86:100–108

    CAS  PubMed  Google Scholar 

  • Lee U, Rioflorido I, Hong S et al (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J 49:115–127

    CAS  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, 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 

  • Li Z, Long R, Zhang T et al (2017) Molecular cloning and functional analysis of the drought tolerance gene MsHSP70 from alfalfa (Medicago sativa L.). J Plant Res 130:387–396

    CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. https://doi.org/10.1042/bst0110591

    Article  CAS  Google Scholar 

  • Liu RH, Meng JL (2003) MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Yi Chuan Hered 25:317–321

    Google Scholar 

  • Liu Z, Liu Y, Shi L et al (2016) SGT1 is required in PcINF1/SRC2-1 induced pepper defense response by interacting with SRC2-1. Sci Rep 6:21651

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller G, Ron Mittler (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288. https://doi.org/10.1093/aob/mcl107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller G, Suzuki N, Rizhsky L et al (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144:1777–1785. https://doi.org/10.1104/pp.107.101436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    CAS  PubMed  Google Scholar 

  • Nakamoto H, Vigh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306

    CAS  PubMed  Google Scholar 

  • Passarinho PA, Van Hengel AJ, Fransz PF, de Vries SC (2001) Expression pattern of the Arabidopsis thaliana AtEP3/AtchitIV endochitinase gene. Planta 212:556–567

    CAS  PubMed  Google Scholar 

  • Prasad TK, Hack E, Hallberg RL (1990) Function of the maize mitochondrial chaperonin hsp60: specific association between hsp60 and newly synthesized F1-ATPase alpha subunits. Mol Cell Biol 10:3979–3986

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi C, Lin X, Li S et al (2019) SoHSC70 positively regulates thermotolerance by alleviating cell membrane damage, reducing ROS accumulation, and improving activities of antioxidant enzymes. Plant Sci 283:385–395. https://doi.org/10.1016/j.plantsci.2019.03.003

    Article  CAS  PubMed  Google Scholar 

  • Qin C, Yu C, Shen Y et al (2014) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc Natl Acad Sci USA 111:5135–5140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rinalducci S, Egidi MG, Mahfoozi S et al (2011) The influence of temperature on plant development in a vernalization-requiring winter wheat: a 2-DE based proteomic investigation. J Proteom 74:643–659

    CAS  Google Scholar 

  • Saibil HR, Fenton WA, Clare DK, Horwich AL (2013) Structure and allostery of the chaperonin GroEL. J Mol Biol 425:1476–1487. https://doi.org/10.1016/j.jmb.2012.11.028

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Maruyama K, Qin F et al (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827

    CAS  PubMed  PubMed Central  Google Scholar 

  • Savić J, Dragićević I, Pantelić D et al (2012) Expression of small heat shock proteins and heat tolerance in potato (Solanum tuberosum L.). Arch Biol Sci (Belgrade) 64:135–144. https://doi.org/10.2298/abs1201135s

    Article  Google Scholar 

  • Schelbert S, Aubry S, Burla B et al (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21:767–785. https://doi.org/10.1105/tpc.108.064089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Proc Bulg Acad Sci 51:121–124

    Google Scholar 

  • Singh RK, Jaishankar J, Muthamilarasan M et al (2016) Genome-wide analysis of heat shock proteins in C 4 model, foxtail millet identifies potential candidates for crop improvement under abiotic stress. Sci Rep 6:32641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su Y, Xu L, Fu Z et al (2014) ScChi, encoding an acidic class III chitinase of sugarcane, confers positive responses to biotic and abiotic stresses in sugarcane. Int J Mol Sci 15:2738–2760

    PubMed  PubMed Central  Google Scholar 

  • Sung D, Kaplan F, Guy CL (2001) Plant Hsp70 molecular chaperones: protein structure, gene family, expression and function. Physiol Plant 113:443–451

    CAS  Google Scholar 

  • Tan W, Wei Meng Q, Brestic M et al (2011) Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J Plant Physiol 168:2063–2071

    CAS  PubMed  Google Scholar 

  • Török Z, Horváth I, Goloubinoff P et al (1997) Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci USA 94:2192–2197. https://doi.org/10.1073/pnas.94.6.2192

    Article  PubMed  PubMed Central  Google Scholar 

  • Tubiello FN, Soussana J-F, Howden SM (2007) Crop and pasture response to climate change. Proc Natl Acad Sci USA 104:19686–19690

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uzilday B, Turkan I, Sekmen AH et al (2012) Comparison of ROS formation and antioxidant enzymes in Cleome gynandra (C4) and Cleome spinosa (C3) under drought stress. Plant Sci 182:59–70. https://doi.org/10.1016/j.plantsci.2011.03.015

    Article  CAS  PubMed  Google Scholar 

  • Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117

    CAS  PubMed  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223. https://doi.org/10.1016/j.envexpbot.2007.05.011

    Article  Google Scholar 

  • Wang L-J, Li S-H (2006) Salicylic acid-induced heat or cold tolerance in relation to Ca2+ homeostasis and antioxidant systems in young grape plants. Plant Sci 170:685–694

    CAS  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    CAS  PubMed  Google Scholar 

  • Wang Y, Lin S, Song Q et al (2014) Genome-wide identification of heat shock proteins (Hsps) and Hsp interactors in rice: Hsp70s as a case study. BMC Genom 15:344

    Google Scholar 

  • Wang X, Zhang H, Shao L-Y et al (2018) Expression and function analysis of a rice OsHSP40 gene under salt stress. Genes Genom 11:1–8. https://doi.org/10.1007/s1325

    Article  Google Scholar 

  • Xu C, Huang B (2010) Comparative analysis of drought responsive proteins in Kentucky bluegrass cultivars contrasting in drought tolerance. Crop Sci 50:2543–2552

    Google Scholar 

  • Yamauchi N, Funamoto Y, Shigyo M (2004) Peroxidase-mediated chlorophyll degradation in horticultural crops. Phytochem Rev 3:221–228. https://doi.org/10.1023/B:PHYT.0000047796.98784.06

    Article  CAS  Google Scholar 

  • Yer EN, Baloglu MC, Ayan S (2018) Identification and expression profiling of all Hsp family member genes under salinity stress in different poplar clones. Gene 678:324–336

    CAS  PubMed  Google Scholar 

  • Yin Y-X, Guo W-L, Zhang Y-L et al (2014) Cloning and characterisation of a pepper aquaporin, CaAQP, which reduces chilling stress in transgenic tobacco plants. Plant Cell Tissue Organ Cult 118:431–444

    CAS  Google Scholar 

  • Young LW, Wilen RW, Bonham-Smith PC (2004) High temperature stress of Brassica napus during flowering reduces micro-and megagametophyte fertility, induces fruit abortion, and disrupts seed production. J Exp Bot 55:485–495

    CAS  PubMed  Google Scholar 

  • Zhang H-X, Jin J-H, He Y-M et al (2016) Genome-wide identification and analysis of the SBP-box family genes under Phytophthora capsici stress in pepper (Capsicum annuum L.). Front Plant Sci 7:504

    PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported through funding from the National Natural Science Foundation of China (no. U1603102) and National Key R&D Program of China (no. 2016YFD0101900)

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Authors and Affiliations

  1. College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, People’s Republic of China

    Saeed ul Haq, Abid Khan, Muhammad Ali, Wen-Xian Gai, Huai-Xia Zhang & Zhen-Hui Gong

  2. Institute of Horticulture Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, 830091, People’s Republic of China

    Qing-Hui Yu & Sheng-Bao Yang

  3. Tianjin Vegetable Research Center, Tianjin, 300192, People’s Republic of China

    Ai-Min Wei

  4. State Key Laboratory of Vegetable Germplasm Innovation, Tianjin, 300384, People’s Republic of China

    Zhen-Hui Gong

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  1. Saeed ul Haq
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Fig. S1

Expression pattern of pepper HSP60 genes under HS treatment (42 °C) at 0, 2, and 8 h in the TRV2:CaHSP60-6 and TRV2:00 pepper R9 plants after VIGS to check the silencing specificity of CaHSP60-6 knockdown. Mean values and SDs are for three replicates, while letters (a–c) represent the significant differences at P < 0.05 (TIFF 80574 kb)

Table S1

Primers for qRT-PCR for CaHSP60 genes (DOCX 15 kb)

Table S2

Primers for gene sequencing and confirmation (DOCX 15 kb)

Table S3

Ten conserved motifs found in pepper HSP60 proteins (DOCX 504 kb)

Table S4

List of Cpn60_TCP1 domain, e value, formulas and total number of atoms of HSP60 genes in pepper (DOCX 16 kb)

Table S5

Detail of the cis-acting elements found in the promoter region of CaHSP60s (DOCX 14 kb)

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Haq, S.u., Khan, A., Ali, M. et al. Knockdown of CaHSP60-6 confers enhanced sensitivity to heat stress in pepper (Capsicum annuum L.). Planta 250, 2127–2145 (2019). https://doi.org/10.1007/s00425-019-03290-4

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