Genome-Wide Characterization and Functional Validation of the ACS Gene Family in the Chestnut Reveals Its Regulatory Role in Ovule Development

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2024 Apr 27

PMID 38674037

Authors

Yanhong Cui

Xingzhou Ji

Wenjie Yu

Yang Liu

Qian Bai

Shuchai Su

Affiliations

Soon will be listed here.

Abstract

Ovule abortion significantly contributes to a reduction in chestnut yield. Therefore, an examination of the mechanisms underlying ovule abortion is crucial for increasing chestnut yield. In our previous study, we conducted a comprehensive multiomic analysis of fertile and abortive ovules and found that genes in chestnuts () play a crucial role in ovule development. Therefore, to further study the function of genes, a total of seven members were identified, their gene structures, conserved structural domains, evolutionary trees, chromosomal localization, and promoter cis-acting elements were analyzed, and their subcellular localization was predicted and verified. The spatiotemporal specificity of the expression of the seven genes was confirmed via qRT-PCR analysis. Notably, was exclusively expressed in the floral organs, and its expression peaked during fertilization and decreased after fertilization. The ACC levels remained consistently greater in fertile ovules than in abortive ovules. The ACSase activity of was identified using the genetic transformation of chestnut healing tissue. Micro plants overexpressing had a significantly greater rate of seed failure than did wild-type plants. Our results suggest that ovule fertilization activates and increases ACC levels, whereas an overexpression of leads to an increase in ACC content in the ovule prior to fertilization, which can lead to abortion. In conclusion, the present study demonstrated that chestnut ovule abortion is caused by poor fertilization and not by nutritional competition. Optimization of the pollination and fertilization of female flowers is essential for increasing chestnut yield and reducing ovule abortion.

References

Letunic I, Khedkar S, Bork P . SMART: recent updates, new developments and status in 2020. Nucleic Acids Res. 2020; 49(D1):D458-D460. PMC: 7778883. DOI: 10.1093/nar/gkaa937. View

Tsuchisaka A, Theologis A . Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 2004; 136(2):2982-3000. PMC: 523360. DOI: 10.1104/pp.104.049999. View

Wang C, Li W, Chen F, Cheng Y, Huang X, Zou B . Genome-Wide Identification and Characterization of Members of the Gene Family in and Their Transcriptional Responses to the Specific Treatments. Int J Mol Sci. 2022; 23(15). PMC: 9369044. DOI: 10.3390/ijms23158476. View

Kawamoto N, Del Carpio D, Hofmann A, Mizuta Y, Kurihara D, Higashiyama T . A Peptide Pair Coordinates Regular Ovule Initiation Patterns with Seed Number and Fruit Size. Curr Biol. 2020; 30(22):4352-4361.e4. DOI: 10.1016/j.cub.2020.08.050. View

Chen C, Wu Y, Li J, Wang X, Zeng Z, Xu J . TBtools-II: A "one for all, all for one" bioinformatics platform for biological big-data mining. Mol Plant. 2023; 16(11):1733-1742. DOI: 10.1016/j.molp.2023.09.010. View

Rowe J, Topping J, Liu J, Lindsey K . Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol. 2016; 211(1):225-39. PMC: 4982081. DOI: 10.1111/nph.13882. View

Cui Y, Ji X, Zhang Y, Liu Y, Bai Q, Su S . Transcriptomic and Metabolic Profiling Reveal the Mechanism of Ovule Development in . Int J Mol Sci. 2024; 25(4). PMC: 10888392. DOI: 10.3390/ijms25041974. View

Zhao Y, Song C, Brummell D, Qi S, Lin Q, Duan Y . Jasmonic acid treatment alleviates chilling injury in peach fruit by promoting sugar and ethylene metabolism. Food Chem. 2020; 338:128005. DOI: 10.1016/j.foodchem.2020.128005. View

Aguado E, Garcia A, Manzano S, Valenzuela J, Cuevas J, Pinillos V . The sex-determining gene CitACS4 is a pleiotropic regulator of flower and fruit development in watermelon (Citrullus lanatus). Plant Reprod. 2018; 31(4):411-426. DOI: 10.1007/s00497-018-0346-1. View

10.

Li D, Flores-Sandoval E, Ahtesham U, Coleman A, Clay J, Bowman J . Ethylene-independent functions of the ethylene precursor ACC in Marchantia polymorpha. Nat Plants. 2020; 6(11):1335-1344. DOI: 10.1038/s41477-020-00784-y. View

11.

Li Q, Guo W, Chen B, Pan F, Yang H, Zhou J . Transcriptional and Hormonal Responses in Ethephon-Induced Promotion of Femaleness in Pumpkin. Front Plant Sci. 2021; 12:715487. PMC: 8442687. DOI: 10.3389/fpls.2021.715487. View

12.

Mou W, Kao Y, Michard E, Simon A, Li D, Wudick M . Ethylene-independent signaling by the ethylene precursor ACC in Arabidopsis ovular pollen tube attraction. Nat Commun. 2020; 11(1):4082. PMC: 7429864. DOI: 10.1038/s41467-020-17819-9. View

13.

Liu S, Lei C, Zhu Z, Li M, Chen Z, He W . Genome-Wide Analysis and Identification of 1-Aminocyclopropane-1-Carboxylate Synthase () Gene Family in Wheat ( L.). Int J Mol Sci. 2023; 24(13). PMC: 10342151. DOI: 10.3390/ijms241311158. View

14.

Gamalero E, Lingua G, Glick B . Ethylene, ACC, and the Plant Growth-Promoting Enzyme ACC Deaminase. Biology (Basel). 2023; 12(8). PMC: 10452086. DOI: 10.3390/biology12081043. View

15.

Wittkopp P, Kalay G . Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet. 2011; 13(1):59-69. DOI: 10.1038/nrg3095. View

16.

Vanderstraeten L, Depaepe T, Bertrand S, Van Der Straeten D . The Ethylene Precursor ACC Affects Early Vegetative Development Independently of Ethylene Signaling. Front Plant Sci. 2019; 10:1591. PMC: 6908520. DOI: 10.3389/fpls.2019.01591. View

17.

Basu D, Tian L, Debrosse T, Poirier E, Emch K, Herock H . Glycosylation of a Fasciclin-Like Arabinogalactan-Protein (SOS5) Mediates Root Growth and Seed Mucilage Adherence via a Cell Wall Receptor-Like Kinase (FEI1/FEI2) Pathway in Arabidopsis. PLoS One. 2016; 11(1):e0145092. PMC: 4701510. DOI: 10.1371/journal.pone.0145092. View

18.

Plett J, Williams M, Leclair G, Regan S, Beardmore T . Heterologous over-expression of ACC SYNTHASE8 (ACS8) in Populus tremula x P. alba clone 717-1B4 results in elevated levels of ethylene and induces stem dwarfism and reduced leaf size through separate genetic pathways. Front Plant Sci. 2014; 5:514. PMC: 4220096. DOI: 10.3389/fpls.2014.00514. View

19.

Arteca J, Arteca R . A multi-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase (ACS6) in mature Arabidopsis leaves. Plant Mol Biol. 1999; 39(2):209-19. DOI: 10.1023/a:1006177902093. View

20.

Xu S, Rahman A, Baskin T, Kieber J . Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell. 2008; 20(11):3065-79. PMC: 2613664. DOI: 10.1105/tpc.108.063354. View