Impairment of root auxin–cytokinins homeostasis induces collapse of incompatible melon grafts during fruit ripening

Maria Dolores Camalle , Aleš Pěnčík , Ondřej Novák , Lina Zhao , Udi Zurgil , Aaron Fait , Noemi Tel-Zur

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac110

PDF (2041KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac110 DOI: 10.1093/hr/uhac110
Article
research-article
Impairment of root auxin–cytokinins homeostasis induces collapse of incompatible melon grafts during fruit ripening
Author information +
History +
PDF (2041KB)

Abstract

The factors underlying the plant collapse of certain melon-pumpkin graft combinations are not fully understood. Our working hypothesis was that impairment of photoassimilates transport in incompatible combinations induces an imbalance in the homeostasis of root auxin (indole-3-acetic acid; IAA) and of cytokinins, probably triggering plant collapse. Root IAA and cytokinins levels in the presence and absence of fruit and changes in root and scion metabolites were investigated in compatible and incompatible combinations. We showed elevated levels of IAA, 2-oxoindole-3-acetic acid (IAA catabolite), indole-3-acetylaspartate (IAA conjugate), and cis-zeatin-type cytokinins, but low levels of trans-zeatin-type cytokinins in the roots of plants of the incompatible combination during fruit ripening. Similarly, during fruit ripening, the expression of the YUCCA genes, YUC2, YUC6, and YUC11 (required for auxin biosynthesis), the GRETCHEN-HAGEN3 gene (required for auxin conjugation), and the cytokinin oxidase/dehydrogenase 7 (CKX7) gene (regulates the irreversible degradation of cytokinin) was enhanced in the roots of plants of the incompatible combination. Moreover, in the incompatible combination the fruiting process restricted transport of photoassimilates to the rootstock and induces their accumulation in the scion. In addition, high levels of hydrogen peroxide and malondialdehyde and reduced activity of antioxidant enzymes were observed in the roots of the incompatible graft. Our results showed that the collapse of the incompatible graft combination during fruit ripening is closely associated with a dramatic accumulation of IAA in the roots, which probably elicits oxidative damage and disturbs the balance of IAA and cytokinins that is of critical importance in melon-pumpkin graft compatibility.

Cite this article

Download citation ▾
Maria Dolores Camalle, Aleš Pěnčík, Ondřej Novák, Lina Zhao, Udi Zurgil, Aaron Fait, Noemi Tel-Zur. Impairment of root auxin–cytokinins homeostasis induces collapse of incompatible melon grafts during fruit ripening. Horticulture Research, 2022, 9 (1) : uhac110 DOI:10.1093/hr/uhac110

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Nisini PT, Colla G, Granati E et al. Rootstock resistance to fusarium wilt and effect on fruit yield and quality of two muskmelon cultivars. Sci Hortic. 2002; 93: 281-8.

[2]

Edelstein M, Ben-Hur M, Cohen R et al. Boron and salinity effects on grafted and non-grafted melon plants. Plant Soil. 2005; 269: 273-84.

[3]

Edelstein M, Plaut Z, Ben-Hur M . Sodium and chloride exclusion and retention by non-grafted and grafted melon and Cucurbita plants. J Exp Bot. 2011; 62: 177-84.

[4]

Wang H, Zhou P, Zhu W et al. De novo comparative transcriptome analysis of genes differentially expressed in the scion of homografted and heterografted tomato seedlings. Sci Rep. 2019; 9: 20240.

[5]

Edelstein M, Cohen R, Burger Y et al. Integrated management of sudden wilt in melons, caused by Monosporascus cannonballus, using grafting and reduced rates of methyl bromide. Plant Dis. 1999; 83: 1142-5.

[6]

Cohen R, Burger Y, Horev C et al. Introducing grafted cucurbits to modern agriculture: the Israeli experience. Plant Dis. 2007; 91: 916-23.

[7]

Minuto A, Bruzzone C, Minuto G et al. The physiological sudden collapse of grafted melon as a result of a not appropriate growing procedure. Acta Hortic. 2010; 883: 229-34.

[8]

Soteriou GA, Papayiannis LC, Kyriacou MC . Indexing melon physiological decline to fruit quality and vine morphometric parameters. Sci Hortic. 2016; 203: 207-15.

[9]

Aloni B, Karni L, Deventurero G et al. Physiological and biochemical changes at the rootstock-scion interface in graft combinations between Cucurbita rootstocks and a melon scion. J Hortic Sci Biotechnol. 2008; 83: 777-83.

[10]

Aloni B, Karni L, Deventurero G et al. Possible mechanisms for graft incompatibility between melon scions and pumpkin rootstocks. Sci Hortic. 2008; 782: 313-24.

[11]

Aloni B, Cohen R, Karni L et al. Hormonal signaling in rootstock- scion interactions. Sci Hortic. 2010; 127: 119-26.

[12]

Camalle MD, Sikron N, Zurgil U et al. Does scion-rootstock compatibility modulate photoassimilate and hormone trafficking through the graft junction in melon-pumpkin graft combinations? Plant Sci. 2021; 306: 110852.

[13]

Kakimoto T . Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol. 2001; 42: 677-85.

[14]

Sakakibara H. Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol. 2006; 57: 431-49.

[15]

Albacete A, Ghanem ME, Martínez-Andújar C et al. Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot. 2008; 59: 4119-31.

[16]

Albacete A, Martínez-Andújar C, Ghanem ME et al. Rootstockmediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato. Plant Cell Environ. 2009; 32: 928-38.

[17]

Dobra J, Motyka V, Dobrev P et al. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J Plant Physiol. 2010; 167: 1360-70.

[18]

Vyroubalova S, Václavíková K, Turecková V et al. Characterization of new maize genes putatively involved in cytokinin metabolism and their expression during osmotic stress in relation to cytokinin levels. Plant Physiol. 2009; 151: 433-47.

[19]

Mackova H, Hronková M, Dobrá J et al. Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot. 2013; 64: 2805-15.

[20]

Normanly J . Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb Perspect Biol. 2010; 2: a001594.

[21]

Normanly J, Slovin JP, Cohen JD . Auxin biosynthesis and metabolism. In: Davies PJ, ed. In Plant Hormones: Biosynthesis, Signal Transduction, Action! Third ed. Springer-Verlag: New York, 2010, 36-62.

[22]

Novak O, Hényková E, Sairanen I et al. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 2012; 72: 523-36.

[23]

Porco S, Pěnčík A, Rashed A et al. Dioxygenase-encoding AtDAO1 gene controls IAA oxidation and homeostasis in Arabidopsis. Proc Natl Acad Sci U S A. 2016; 113: 11016-21.

[24]

Ljun K, Hul AK, Kowalczyk M et al. Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol. 2002; 50: 309-32.

[25]

Ludwig-Muller J . Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot. 2011; 62: 1757-73.

[26]

Mellor N, Band LR, Pěnčík A et al. Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. Proc Natl Acad Sci U S A. 2016; 113: 11022-7.

[27]

Zhao Y, Christensen SK, Fankhauser C et al. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science. 2001; 291: 306-9.

[28]

Ljung K, Hull AK, Kowalczyk M et al. Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol. 2002; 49: 249-72.

[29]

Won C, Shen X, Mashiguchi K et al. Conversion of tryptophan to indole-3-acetic acid by tryptophan aminotransferases of Arabidopsis and YUCCAs in Arabidopsis. Proc Natl Acad Sci U S A. 2011; 108: 18518-23.

[30]

Bishopp A, Help H, El-Showk S et al. . A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol. 2011; 21: 917-26.

[31]

Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F et al. Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants (Basel). 2020; 9: 1-52.

[32]

Martínez-Ballesta MC, Alcaraz-López C, Muries B et al. Physiological aspects of rootstock-scion interactions. Sci Hortic. 2010; 127: 112-8.

[33]

Edelstein M, Burger Y, Horev C et al. Assessing the effect of genetic and anatomic variation of Cucurbita rootstocks on vigour, survival and yield of grafted melons. J Hortic Sci Biotechnol. 2004; 79: 370-4.

[34]

Mittler R . ROS are good. Trends Plant Sci. 2017; 22: 11-9.

[35]

Li CY, Weiss D, Goldschmidt EE . Effects of carbohydrate starvation on gene expression in citrus root. Planta. 2003; 217: 11-20.

[36]

Yamasaki A, Yamashita M, Furuya S . Mineral concentrations and cytokinin activity in the xylem exudate of grafted watermelons as affected by rootstocks and crop load. J Jpn Soc Hortic Sci. 1994; 62: 817-26.

[37]

Kollmer I, Novak O, Strnad M et al. Overexpression of the cytosolic cytokinin oxidase/dehydrogenase (CKX7) from Arabidopsis causes specific changes in root growth and xylem differentiation. Plant J. 2014; 78: 359-71.

[38]

Di Marzo, Herrera-Ubaldo H, Caporali E et al. SEEDSTICK controls Arabidopsis fruit size by regulating cytokinin levels and FRUITFULL. Cell Rep. 2020; 30: 2846-2857.e3.

[39]

Zhao Y . Essential roles of local auxin biosynthesis in plant development and in adaptation to environmental changes. Annu Rev Plant Biol. 2018; 69: 417-35

[40]

Sorce C, Massai R, Picciarelli P et al. Hormonal relationships in xylem sap of grafted and ungrafted Prunus rootstocks. Sci Hortic. 2002; 93: 333-42.

[41]

Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002; 7: 405-10.

[42]

Peer WA, Cheng Y, Murphy AS . Evidence of oxidative attenuation of auxin signalling. J Exp Bot. 2013; 64: 2629-39.

[43]

Ivanchenko G, den Os D, Monshausen GB et al. Auxin increases the hydrogen peroxide (H2O2) concentration in tomato (Solanum lycopersicum) root tips while inhibiting root growth . Ann Bot. 2013; 112: 1107-16.

[44]

Arora A, Sairam RK, Srivastava GC . Oxidative stress and antioxidative system in plants. Curr Sci India. 2002; 82: 1227-38.

[45]

Jajic I, Sarna T, Strzalka K . Senescence, stress, and reactive oxygen species. Plants (Basel). 2015; 4: 393-411.

[46]

Sofo A, Scopa A, Nuzzaci M et al. Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci. 2015; 16: 13561-78.

[47]

Eckardt NA . A new chlorophyll degradation pathway. Plant Cell. 2009; 21: 700.

[48]

Camalle M, Standing D, Jitan M et al. Effect of salinity and nitrogen sources on the leaf quality, biomass, and metabolic responses of two ecotypes of Portulaca oleracea. Agronomy. 2020; 10: 656.

[49]

Wintermans JF, De Mots A . Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim Biophys Acta. 1965; 109: 448-53.

[50]

Svacinova J, Novák O, Plačková L et al. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods. 2012; 8: 17.

[51]

Plackova L, Oklestkova J, Pospíšková K et al. Microscale magnetic microparticle-based immunopurification of cytokinins from Arabidopsis root apex. Plant J. 2017; 89: 1065-75.

[52]

Rittenberg D, Foster L . A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J Biol Chem. 1940; 133: 727-44.

[53]

Srivastava S, Brychkova G, Yarmolinsky D et al. Aldehyde oxidase 4 plays a critical role in delaying silique senescence by catalyzing aldehyde detoxification. Plant Physiol. 2017; 173: 1977-97.

[54]

Mika A, Luthje S . Properties of guaiacol peroxidase activities isolated from corn root plasma membranes. Plant Physiol. 2003; 132: 1489-98.

[55]

Cheng H, Kong W, Hou D et al. Isolation, characterization, and expression analysis of CmMLO2 in muskmelon. Mol Biol Rep. 2013; 40: 2609-15.

PDF (2041KB)

65

Accesses

0

Citation

Detail

Sections
Recommended

/