Competition between anthocyanin and kaempferol glycosides biosynthesis affects pollen tube growth and seed set of Malus

Weifeng Chen , Zhengcao Xiao , Yule Wang , Jinxiao Wang , Rui Zhai , Kui Lin-Wang , Richard Espley , Fengwang Ma , Pengmin Li

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 173

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :173 DOI: 10.1038/s41438-021-00609-9
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Competition between anthocyanin and kaempferol glycosides biosynthesis affects pollen tube growth and seed set of Malus
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Abstract

Flavonoids play important roles in regulating plant growth and development. In this study, three kaempferol 3-O-glycosides were identified and mainly accumulated in flowers but not in leaves or fruits of Malus. In Malus, flower petal color is normally white, but some genotypes have red flowers containing anthocyanin. Anthocyanin biosynthesis appears to be in competition with kaempferol 3-O-glycosides production and controlled by the biosynthetic genes. The white flower Malus genotypes had better-developed seeds than the red flower genotypes. In flowers, the overexpression of MYB10 in Malus domestica enhanced the accumulation of anthocyanin, but decreased that of kaempferol 3-O-glycosides. After pollination the transgenic plants showed slower pollen tube growth and fewer developed seeds. Exogenous application of different flavonoid compounds suggested that kaempferol 3-O-glycosides, especially kaempferol 3-O-rhamnoside, regulated pollen tube growth and seed set rather than cyanidin or quercetin 3-O-glycosides. It was found that kaempferol 3-O-rhamnoside might regulate pollen tube growth through effects on auxin, the Rho of plants (ROP) GTPases, calcium and the phosphoinositides signaling pathway. With the inhibition of auxin transport, the transcription levels of Heat Shock Proteins (HSPs) and ROP GTPases were downregulated while the levels were not changed or even enhanced when blocking calcium signaling, suggesting that HSPs and ROP GTPases were downstream of auxin signaling, but upstream of calcium signaling. In summary, kaempferol glycoside concentrations in pistils correlated with auxin transport, the transcription of HSPs and ROP GTPases, and calcium signaling in pollen tubes, culminating in changes to pollen tube growth and seed set.

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Weifeng Chen, Zhengcao Xiao, Yule Wang, Jinxiao Wang, Rui Zhai, Kui Lin-Wang, Richard Espley, Fengwang Ma, Pengmin Li. Competition between anthocyanin and kaempferol glycosides biosynthesis affects pollen tube growth and seed set of Malus. Horticulture Research, 2021, 8 (1) : 173 DOI:10.1038/s41438-021-00609-9

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References

[1]

Winkel-Shirley, B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126, 485-493 (2001).

[2]

Dare, A. P. et al. Overexpression of chalcone isomerase in apple reduces phloridzin accumulation and increases susceptibility to herbivory by two-spotted mites. Plant J. 103, 293-307 (2020).

[3]

Han, Y. et al. Ectopic expression of apple F3’H genes contributes to anthocyanin accumulation in the Arabidopsis tt7 mutant grown under nitrogen stress. Plant Physiol. 153, 806-820 (2010).

[4]

Colanero, S., Perata, P. & Gonzali, S. What’s behind purple tomatoes? Insight into the mechanisms of anthocyanin synthesis in tomato fruits. Plant Physiol. 182, 1841-1853 (2020).

[5]

Mori, S., Kobayashi, H., Hoshi, Y., Kondo, M. & Nakano, M. Heterologous expression of the flavonoid 3’5’-hydroxylase gene of Vinca major alters flower color in transgenic Petunia hybrida. Plant Cell Rep. 22, 415-421 (2004).

[6]

Grotewold, E . The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol. 57, 761-780 (2006).

[7]

Sheehan, H. et al. MYB-FL controls gain and loss of floral UV absorbance, a key trait affecting pollinator preference and reproductive isolation. Nat. Genet. 48, 159-166 (2016).

[8]

Davies, K. M. et al. Enhancing anthocyanin production by altering competition for substrate between flavonol synthase and dihydroflavonol 4-reductase. Euphytica 131, 259-268 (2003).

[9]

Shirley, B. W., Hanley, S. & Goodman, H. M. Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations. Plant Cell 4, 333-347 (1992).

[10]

Sun, W. et al. Molecular and biochemical analysis of chalcone synthase from Freesia hybrid in flavonoid biosynthetic pathway. PLoS ONE 10, e0119054 (2015).

[11]

Yuan, Y. W., Rebocho, A. B., Sagawa, J. M., Stanley, L. E. & Bradshaw, H. D. Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species. Proc. Natl Acad. Sci. USA 113, 2448-2453 (2016).

[12]

Dare, A. P. et al. Phenotypic changes associated with RNA interference silencing of chalcone synthase in apple (Malus × domestica). Plant J. 74, 398-410 (2013).

[13]

Dare, A. P. et al. Silencing a phloretin-specific glycosyltransferase perturbs both general phenylpropanoid biosynthesis and plant development. Plant J. 91, 237-250 (2017).

[14]

Watkins, J. M., Hechler, P. J. & Muday, G. K. Ethylene-induced flavonol accumulation in guard cells suppresses reactive oxygen species and moderates stomatal aperture. Plant Physiol. 164, 1707-1717 (2014).

[15]

Watkins, J. M., Chapman, J. M. & Muday, G. K. Abscisic acid-induced reactive oxygen species are modulated by flavonols to control stomata aperture. Plant Physiol. 175, 1807-1825 (2017).

[16]

Buer, C. S. & Muday, G. K. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16, 1191-1205 (2004).

[17]

Buer, C. S., Kordbacheh, F., Truong, T. T., Hocart, C. H. & Djordjevic, M. A. Alteration of flavonoid accumulation patterns in transparent testa mutants disturbs auxin transport, gravity responses, and imparts long-term effects on root and shoot architecture. Planta 238, 171-189 (2013).

[18]

Lewis, D. R. et al. Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol. 156, 144-164 (2011).

[19]

Kuhn, B. et al. 7-rhamnosylated flavonols modulate homeostasis of the plant hormone auxin and affect plant development. J. Biol. Chem. 291, 5385-5395 (2016).

[20]

Ringli, C. et al. The modified flavonol glycosylation profile in the Arabidopsis rol1 mutants results in alterations in plant growth and cell shape formation. Plant Cell 20, 1470-1481 (2008).

[21]

Lan, X. et al. Flavonoids and ROS play opposing roles in mediating pollination in ornamental kale (Brassica oleracea var. acephala). Mol. Plant 10, 1361-1364 (2017).

[22]

Chen, J., Ullah, C., Reichelt, M., Gershenzon, J. & Hammerbacher, A. Sclerotinia sclerotiorum circumvents flavonoid defenses by catabolizing flavonol glycosides and aglycones. Plant Physiol. 180, 1975-1987 (2019).

[23]

Muhlemann, J. K., Younts, T. L. & Muday, G. K. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. Proc. Natl Acad. Sci. USA 115, E11188-E11197 (2018).

[24]

Yin, R. et al. Kaempferol 3-O-rhamnoside-7-O-rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots. N. Phytol. 201, 466-475 (2014).

[25]

Xiao, Z. et al. Extraction, identification, and antioxidant and anticancer tests of seven dihydrochalcones from Malus ‘Red Splendor’ fruit. Food Chem. 231, 324-331 (2017).

[26]

Xiao, Z., Wang, Y., Wang, J., Li, P. & Ma, F. Structure-antioxidant capacity relationship of dihydrochalcone compounds in Malus. Food Chem. 275, 354-360 (2019).

[27]

Cornille, A. et al. A multifaceted overview of apple tree domestication. Trends Plant Sci. 24, 770-782 (2019).

[28]

Cornille, A., Giraud, T., Smulders, M. J., Roldán-Ruiz, I. & Gladieux, P. The domestication and evolutionary ecology of apples. Trends Genet. 30, 57-65 (2014).

[29]

Duan, N. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat. Comm. 8, 249 (2017).

[30]

Espley, R. V. et al. Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell 21, 168-183 (2009).

[31]

Espley, R. V. et al. Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J. 49, 414-427 (2007).

[32]

Shivanna, K. R. & Rangaswamy, N. S. (eds). Pollen Biology, a Laboratory Manual (Springer-Verlag 1992)

[33]

Tian, J. et al. McMYB10 regulates coloration via activating McF3′H and later structural genes in ever-red leaf crabapple. Plant Biot. J. 13, 948-961 (2015).

[34]

Meng, D. et al. Decreased sorbitol synthesis leads to abnormal stamen development and reduced pollen tube growth via an MYB transcription factor, MdMYB39L, in apple (Malus domestica). N. Phytol. 217, 641-656 (2018).

[35]

Guan, Y., Guo, J., Li, H. & Yang, Z. Signaling in pollen tube growth: crosstalk, feedback, and missing links. Mol. Plant 6, 1053-1064 (2013).

[36]

Takeuchi, H. & Higashiyama, T. Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531, 245-248 (2016).

[37]

Feng, Q. N., Liang, X., Li, S. & Zhang, Y. The ADAPTOR PROTEIN-3 complex mediates pollen tube growth by coordinating vacuolar targeting and organization. Plant Physiol. 177, 216-225 (2018).

[38]

Chen, D. & Zhao, J. Free IAA in stigmas and styles during pollen germination and pollen tube growth of Nicotiana tabacum. Physiol. Plant. 134, 202-215 (2008).

[39]

Wu, J. Z., Lin, Y., Zhang, X. L., Pang, D. W. & Zhao, J. IAA stimulates pollen tube growth and mediates the modification of its wall composition and structure in Torenia fournieri. J. Exp. Bot. 59, 2529-2543 (2008).

[40]

Dal Bosco, C. et al. The endoplasmic reticulum localized PIN8 is a pollen-specific auxin carrier involved in intracellular auxin homeostasis. Plant J. 71, 860-870 (2012).

[41]

Ding, Z. et al. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Comm. 3, 941 (2012).

[42]

Rieu, I., Twell, D. & Firon, N. Pollen development at high temperature: from acclimation to collapse. Plant Physiol. 173, 1967-1976 (2017).

[43]

Qin, Y. et al. Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet. 5, e1000621 (2009).

[44]

Vogt, T., Pollak, P., Tarlyn, N. & Taylor, L. P. Pollination-or wound-induced kaempferol accumulation in petunia stigmas enhances seed production. Plant Cell 6, 11-23 (1994).

[45]

Ylstra, B. et al. Flavonols stimulate development, germination, and tube growth of tobacco pollen. Plant Physiol. 100, 902-907 (1992).

[46]

Kevan, P., Giurfa, M. & Chittka, L. Why are there so many and so few white flowers? Trends Plant Sci. 1, 252 (1996).

[47]

Dag, A., Stern, R. A. & Shafir, S. Honey bee (Apis mellifera) strains differ in apple (Malus domestica) pollen foraging preference. J. Apic. Res. 44, 15-20 (2005).

[48]

Garratt, M. P. D. et al. Apple pollination: demand depends on variety and supply depends on pollinator identity. PLoS ONE 11, e0153889 (2016).

[49]

Ramírez, F. & Davenport, T. L. Apple pollination: a review. Sci. Hortic. 162, 188-203 (2013).

[50]

Dai, H. et al. Development of a seedling clone with high regeneration capacity and susceptibility to Agrobacterium in apple. Sci. Hortic. 164, 202-208 (2013).

[51]

Li, P., Ma, F. & Cheng, L. Primary and secondary metabolism in the sun-exposed peel and the shaded peel of apple fruit. Physiol. Plant. 148, 9-24 (2013).

[52]

Malnoy, M., Reynoird, J. P., Mourgues, F., Chevreau, E. & Simoneau, P. A method for isolating total RNA from pear leaves. Plant Mol. Biol. Rep. 19, 69a-69f (2001).

[53]

Kho, Y. O. & Baer, J. Observing pollen tubes by means of fluorescence. Euphytica 17, 298-302 (1968).

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