A multi-omics approach identifies bHLH71-like as a positive regulator of yellowing leaf pepper mutants exposed to high-intensity light

Zhoubin Liu , Lianzhen Mao , Bozhi Yang , Qingzhi Cui , Yunhua Dai , Xueqiao Li , Yisong Chen , Xiongze Dai , Xuexiao Zou , Lijun Ou , Sha Yang

Horticulture Research ›› 2023, Vol. 10 ›› Issue (7) : 098

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (7) :098 DOI: 10.1093/hr/uhad098
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A multi-omics approach identifies bHLH71-like as a positive regulator of yellowing leaf pepper mutants exposed to high-intensity light
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Abstract

Light quality and intensity can have a significant impact on plant health and crop productivity. Chlorophylls and carotenoids are classes of plant pigments that are responsible for harvesting light energy and protecting plants from the damaging effects of intense light. Our understanding of the role played by plant pigments in light sensitivity has been aided by light-sensitive mutants that change colors upon exposure to light of variable intensity. In this study, we conducted transcriptomic, metabolomic, and hormone analyses on a novel yellowing mutant of pepper (yl1) to shed light on the molecular mechanism that regulates the transition from green to yellow leaves in this mutant upon exposure to high-intensity light. Our results revealed greater accumulation of the carotenoid precursor phytoene and the carotenoids phytofluene, antheraxanthin, and zeaxanthin in yl1 compared with wild-type plants under high light intensity. A transcriptomic analysis confirmed that enzymes involved in zeaxanthin and antheraxanthin biosynthesis were upregulated in yl1 upon exposure to high-intensity light. We also identified a single basic helix–loop–helix (bHLH) transcription factor, bHLH71-like, that was differentially expressed and positively correlated with light intensity in yl1. Silencing of bHLH71-like in pepper plants suppressed the yellowing phenotype and led to reduced accumulation of zeaxanthin and antheraxanthin. We propose that the yellow phenotype of yl1 induced by high light intensity could be caused by an increase in yellow carotenoid pigments, concurrent with a decrease in chlorophyll accumulation. Our results also suggest that bHLH71-like functions as a positive regulator of carotenoid biosynthesis in pepper.

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Zhoubin Liu, Lianzhen Mao, Bozhi Yang, Qingzhi Cui, Yunhua Dai, Xueqiao Li, Yisong Chen, Xiongze Dai, Xuexiao Zou, Lijun Ou, Sha Yang. A multi-omics approach identifies bHLH71-like as a positive regulator of yellowing leaf pepper mutants exposed to high-intensity light. Horticulture Research, 2023, 10 (7) : 098 DOI:10.1093/hr/uhad098

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Acknowledgements

This research was funded by the Special Project of Biological Seed Industry and Fine and Deep Processing of Agricultural Products (grant 202202AE090031), the Project of Education Department of Hunan Province (grant 22B0229), and the Key Research and Development Program of Hainan Province (grant ZD2020060).

Author contributions

Conceptualization, S.Y. and L.O.; methodology, Z.L., B.Y. and L.M.; formal analysis, Z.L. and L.M.; investigation, Y.D., X.L., and Y.C.; writing the original draft, Z.L. and L.M.; review and editing of the draft, X.D. and S.Y.; visualization, Z.L. and Q.C.; funding acquisition, X.Z. and L.O.

Data availability

RNA-seq data generated in this study are available at the NCBI Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra) under accession number PRJNA771934.

Conflict of interest

None declared.

References

[1]

Susila H, Jin S, Ahn JH . Light intensity and floral transition: chloroplast says "time to flower!". Mol Plant. 2016; 9: 1551-3.

[2]

Chen M, Chory J, Fankhauser C . Light signal transduction in higher plants. Annu Rev Genet. 2004; 38: 87-117.

[3]

Wang W, Liu D, Qin M et al. Effects of supplemental lighting on potassium transport and fruit coloring of tomatoes grown in hydroponics. Int J Mol Sci. 2021; 22: 2687.

[4]

Yasui Y, Mukougawa K, Uemoto M et al. The phytochrome-interacting vascular plant one-zinc finger1 and VOZ2 redundantly regulate flowering in Arabidopsis. Plant Cell. 2012; 24: 3248-63.

[5]

Liu H, Yu X, Li K et al. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science. 2008; 322: 1535-9.

[6]

Quian-Ulloa R, Stange C . Carotenoid biosynthesis and plastid development in plants: the role of light. Int J Mol Sci. 2021; 22: 1184.

[7]

Albrecht M, Sandmann G . Light-stimulated carotenoid biosynthesis during transformation of maize etioplasts is regulated by increased activity of isopentenyl pyrophosphate isomerase. Plant Physiol. 1994; 105: 529-34.

[8]

Von LJ, Welsch R, Bonk M et al. Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. Plant J. 1997; 12: 625-34.

[9]

Fuentes P, Pizarro L, Moreno JC et al. Light-dependent changes in plastid differentiation influence carotenoid gene expression and accumulation in carrot roots. Plant Mol Biol. 2012; 79: 47-59.

[10]

Meier S, Tzfadia O, Vallabhaneni R et al. A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst Biol. 2011; 5: 77.

[11]

Tian Y, Rao S, Li Q et al. The coloring mechanism of a novel golden variety in Populus deltoides based on the RGB color mode. Forestry Res. 2021; 1: 5.

[12]

Bi W, Gao Y, Shen J et al. PG traditional uses phytochemistry and pharmacology of the genus Acer (maple): a review. J Ethnopharmacol. 2016; 189: 31-60.

[13]

Wang ZX, Yu YF, Chen L et al. Advances in leaf pigment composition, structure and photosynthetic characteristics of colored-leaf plants. Plant Physiol J. 2016; 52: 1-7.

[14]

Hashimoto H, Uragami C, Cogdell RJ . Carotenoids and photosynthesis. Subcell Biochem. 2016; 79: 111-39.

[15]

Marles M, Gruber MY, Scoles GJ et al. Pigmentation in the developing seed coat and seedling leaves of Brassica carinata is controlled at the dihydroflavonol reductase locus. Phytochemistry. 2003; 62: 663-72.

[16]

Zhang K, Liu ZY, Shan XF et al. Physiological properties and chlorophyll biosynthesis in a Pak-choi (Brassica rapa L. ssp. chinensis) yellow leaf mutant, pylm. Acta Physiol Plant. 2017; 39: 1-10.

[17]

Xu J, Yang J, Wu Z et al. Identification of a dual-targeted protein belonging to the mitochondrial carrier family that is required for early leaf development in rice. Plant Physiol. 2013; 161: 2036-48.

[18]

Ma X, Sun X, Li C et al. Map-based cloning and characterization of the novel yellow-green leaf gene ys83 in rice (Oryza sativa). Plant Physiol Biochem. 2017; 111: 1-9.

[19]

Zhang T, Feng P, Li Y et al. VIRESCENT-ALBINO LEAF 1 regulates LEAF colour development and cell division in rice. J Exp Bot. 2018; 69: 4791-804.

[20]

Li QZ, Zhu FY, Gao XL et al. Young leaf chlorosis 2 encodes the stroma-localized heme oxygenase 2 which is required for normal tetrapyrrole biosynthesis in rice. Planta. 2014; 240: 701-12.

[21]

Liu X, Lan J, Huang Y et al. WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress. J Exp Bot. 2018; 69: 3949-61.

[22]

Luo T, Luo S, Araujo WL et al. Virus-induced gene silencing of pea CHLI and CHLD affects tetrapyrrole biosynthesis, chloroplast development and the primary metabolic network. Plant Physiol Biochem. 2013; 65: 17-26.

[23]

Nisar N, Li L, Lu S et al. Carotenoid metabolism in plants. Mol Plant. 2015; 8: 68-82.

[24]

Sun T, Yuan H, Cao H et al. Carotenoid metabolism in plants: the role of plastids. Mol Plant. 2018; 11: 58-74.

[25]

Hirschberg J . Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol. 2001; 4: 210-8.

[26]

Moreno JC, Mi J, Agrawal S et al. Expression of a carotenogenic gene allows faster biomass production by redesigning plant architecture and improving photosynthetic efficiency in tobacco. Plant J. 2020; 103: 1967-84.

[27]

Yin W, Hu Z, Cui B et al. Suppression of the MADS-box gene SlMBP8 accelerates fruit ripening of tomato (Solanum lycopersicum). Plant Physiol Biochem. 2017; 118: 235-44.

[28]

Zhu F, Luo T, Liu C et al. An R2R3-MYB transcription factor represses the transformation of α- and β-branch carotenoids by negatively regulating expression of CrBCH2 and CrNCED5 in flavedo of Citrus reticulate. New Phytol. 2017; 216: 178-92.

[29]

Toledo-Ortiz G, Johansson H, Lee KP et al. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet. 2014; 10: 1004416.

[30]

Zhu Z, Chen G, Guo X et al. Overexpression of SlPRE2, an atypical bHLH transcription factor, affects plant morphology and fruit pigment accumulation in tomato. Sci Rep. 2017; 7: 57-86.

[31]

Zhou D, Shen Y, Zhou P et al. Papaya CpbHLH1/2 regulate carotenoid biosynthesis-related genes during papaya fruit ripening. Hortic Res. 2019; 6: 80.

[32]

Hu S, Liu L, Li S et al. Regulation of fruit ripening by the brassinosteroid biosynthetic gene SlCYP90B3 via an ethylene-dependent pathway in tomato. Hortic Res. 2020; 7: 163.

[33]

Sun T, Rao S, Zhou X et al. Plant carotenoids: recent advances and future perspectives. Mol Hortic. 2022; 2: 3.

[34]

Ernesto BR, Silvestre LB, Santos MS et al. Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato. J Exp Bot. 2018; 69: 3573-86.

[35]

Zhang Z, Liu Y, Yuan Q et al. The bHLH1-DTX35/DFR module regulates pollen fertility by promoting flavonoid biosynthesis in Capsicum annuum L. Hortic Res. 2022; 9: 172.

[36]

Lunch CK, Lafountain AM, Thomas S et al. The xanthophyll cycle and NPQ in diverse desert and aquatic green algae. Photosynth Res. 2013; 115: 139-51.

[37]

Vaz J, Sharma PK . Relationship between xanthophyll cycle and non-photochemical quenching in rice (Oryza sativa L.) plants in response to light stress. Indian J Exp Biol. 2011; 49: 60-7.

[38]

Cazzonelli CI, Pogson BJ . Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 2010; 15: 266-74.

[39]

Shi Y, Wei P, Liu F et al. Cloning and expression analysis of violaxanthin de-epoxidase gene in Nicotiana tabacum. Tob Sci Technol. 2014; 47: 27-33.

[40]

Janik E, Bednarska J, Zubik M et al. The xanthophyll cycle pigments, violaxanthin and zeaxanthin, modulate molecular organization of the photosynthetic antenna complex LHCII. Arch Biochem Biophys. 2016; 592: 1-9.

[41]

Chen C, Li H, Zhang D et al. The role of anthocyanin in photoprotection and its relationship with the xanthophyll cycle and the antioxidant system in apple peel depends on the light conditions. Physiol Plant. 2013; 163: 354-62.

[42]

de Lucas M, Prat S . PIFs get BRright: PHYTOCHROME INTERACTING FACTORs as integrators of light and hormonal signals. New Phytol. 2014; 202: 1126-41.

[43]

Goh CH, Lee DJ, Bae HJ . Gibberellic acid of Arabidopsis regulates the abscisic acid-induced inhibition of stomatal opening in response to light. Plant Sci. 2009; 176: 136-42.

[44]

Ross J, O’Neill D . New interactions between classical plant hormones. Trends Plant Sci. 2001; 6: 2-4.

[45]

Nagashima A, Suzuki G, Uehara Y et al. Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. Plant J. 2010; 53: 516-29.

[46]

Khan W, Prithiviraj B, Smith DL . Photosynthetic responses of corn and soybean to foliar application of salicylates. J Plant Physiol. 2003; 160: 485-92.

[47]

Tian L, Dellapenna D, Zeevaart J . Effect of hydroxylated carotenoid deficiency on ABA accumulation in Arabidopsis. Physiol Plant. 2010; 122: 314-20.

[48]

Llorente B, D’Andrea L, Ruiz-Sola MA et al. Tomato fruit carotenoid biosynthesis is adjusted to actual ripening progression by a light-dependent mechanism. Plant J. 2016; 85: 107-19.

[49]

Mao L, Dai Y, Huang Y et al. Effect of light intensity on gene expression in hypocotyl during the elongation in a leaf-yellowing mutant of pepper (Capsicum annuum L.). Agronomy. 2022; 12: 2762.

[50]

Kanehisa M, Araki M, Goto S et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2007; 36: D480-4.

[51]

Young MD, Wakefield MJ, Smyth GK et al. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010; 11: R14-2.

[52]

Chen C, Chen H, Zhang Y et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13: 1194-202.

[53]

Taylor SC, Nadeau K, Abbasi M et al. The ultimate qPCR experiment: producing publication quality, reproducible data the first time. Trends Biotechnol. 2019; 37: 761-74.

[54]

Mestdagh P, Van Vlierberghe P, De Weer A et al. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 2009; 10: R64.

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