Genome-wide investigation and expression profiling of  APX  gene family in  Gossypium hirsutum  provide new insights in redox homeostasis maintenance during different fiber development stages

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Abstract

Ascorbate peroxidase (APX) is a member of heme-containing peroxidases which catalyze the H ₂O ₂-dependent oxidation of a wide range of substrates in plants and animals. As is known, H ₂O ₂ acts as a signaling molecule in the regulation of fiber development. Our previous work reported that ascorbate peroxidase 1 ( GhAPX1) was important for cotton fiber elongation. However, knowledge about APX gene family members and their evolutionary and functional characteristics in cotton is limited. Here, we report 26 GhAPX genes by genome-wide investigation of tetraploid cotton Gossypium hirsutum. Phylogenetic and gene structure analyses classified these APX members into five clades and syntenic analysis suggested two duplication events. Expression profiling of the 26 APXs revealed that ten members are expressed in cotton fibers. Notably, GhAPX10A, GhAPX10D, GhAPX12A, and GhAPX12D showed high expression levels in 30-day fiber, while GhAPX1A/ D, GhAPX3A/ D, and GhAPX6A/ D showed very low expression levels. The enzyme activity and H ₂O ₂ content assays revealed that cotton fiber kept high enzyme activity and the lowest H ₂O ₂ level in 30-day fibers, indicating that other than GhAPX1, the newly reported APX members are responsible for the reactive oxygen species homeostasis in the cotton fiber maturation stages. Expression profiling of ten fiber-expressed APXs after phytohormone treatments revealed their regulation patterns by different stimuli, suggesting that GhAPX1, GhAPX12A, and GhAPX12D are responsible to most phytohormone treatments. Our data provided evolutionary and functional information of GhAPX gene family members and revealed that different members are responsible to redox homeostasis during different cotton fiber development stages.

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Most cited references 38

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Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.

Z. M. Pei, Y Murata, G. Benning … (2000)

Drought is a major threat to agricultural production. Plants synthesize the hormone abscisic acid (ABA) in response to drought, triggering a signalling cascade in guard cells that results in stomatal closure, thus reducing water loss. ABA triggers an increase in cytosolic calcium in guard cells ([Ca2+]cyt) that has been proposed to include Ca2+ influx across the plasma membrane. However, direct recordings of Ca2+ currents have been limited and the upstream activation mechanisms of plasma membrane Ca2+ channels remain unknown. Here we report activation of Ca2+-permeable channels in the plasma membrane of Arabidopsis guard cells by hydrogen peroxide. The H2O2-activated Ca2+ channels mediate both influx of Ca2+ in protoplasts and increases in [Ca2+]cyt in intact guard cells. ABA induces the production of H2O2 in guard cells. If H2O2 production is blocked, ABA-induced closure of stomata is inhibited. Moreover, activation of Ca2+ channels by H2O2 and ABA- and H2O2-induced stomatal closing are disrupted in the recessive ABA-insensitive mutant gca2. These data indicate that ABA-induced H2O2 production and the H2O2-activated Ca2+ channels are important mechanisms for ABA-induced stomatal closing.

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Photosynthesis and drought: can we make metabolic connections from available data?

C. Pinheiro, M. Chaves (2011)

Photosynthesis is one of the key processes to be affected by water deficits, via decreased CO2 diffusion to the chloroplast and metabolic constraints. The relative impact of those limitations varies with the intensity of the stress, the occurrence (or not) of superimposed stresses, and the species we are dealing with. Total plant carbon uptake is further reduced due to the concomitant or even earlier inhibition of growth. Leaf carbohydrate status, altered directly by water deficits or indirectly (via decreased growth), acts as a metabolic signal although its role is not totally clear. Other relevant signals acting under water deficits comprise: abscisic acid (ABA), with an impact on stomatal aperture and the regulation at the transcription level of a large number of genes related to plant stress response; other hormones that act either concurrently (brassinosteroids, jasmonates, and salycilic acid) or antagonistically (auxin, cytokinin, or ethylene) with ABA; and redox control of the energy balance of photosynthetic cells deprived of CO2 by stomatal closure. In an attempt to systematize current knowledge on the complex network of interactions and regulation of photosynthesis in plants subjected to water deficits, a meta-analysis has been performed covering >450 papers published in the last 15 years. This analysis shows the interplay of sugars, reactive oxygen species (ROS), and hormones with photosynthetic responses to drought, involving many metabolic events. However, more significantly it highlights (i) how fragmented and often non-comparable the results are and (ii) how hard it is to relate molecular events to plant physiological status, namely photosynthetic activity, and to stress intensity. Indeed, the same data set usually does not integrate these different levels of analysis. Considering these limitations, it was hard to find a general trend, particularly concerning molecular responses to drought, with the exception of the genes ABI1 and ABI3. These genes, irrespective of the stress type (acute versus chronic) and intensity, show a similar response to water shortage in the two plant systems analysed (Arabidopsis and barley). Both are associated with ABA-mediated metabolic responses to stress and the regulation of stomatal aperture. Under drought, ABI1 transcription is up-regulated while ABI3 is usually down-regulated. Recently ABI3 has been hypothesized to be essential for successful drought recovery.

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Regulation and function of ascorbate peroxidase isoenzymes.

Shigeru Shigeoka, Takahiro Ishikawa, Masahiro Tamoi … (2002)

Even under optimal conditions, many metabolic processes, including the chloroplastic, mitochondrial, and plasma membrane-linked electron transport systems of higher plants, produce active oxygen species (AOS). Furthermore, the imposition of biotic and abiotic stress conditions can give rise to excess concentrations of AOS, resulting in oxidative damage at the cellular level. Therefore, antioxidants and antioxidant enzymes function to interrupt the cascades of uncontrolled oxidation in each organelle. Ascorbate peroxidase (APX) exists as isoenzymes and plays an important role in the metabolism of H(2)O(2) in higher plants. APX is also found in eukaryotic algae. The characterization of APX isoenzymes and the sequence analysis of their clones have led to a number of investigations that have yielded interesting and novel information on these enzymes. Interestingly, APX isoenzymes of chloroplasts in higher plants are encoded by only one gene, and their mRNAs are generated by alternative splicing of the gene's two 3'-terminal exons. Manipulation of the expression of the enzymes involved in the AOS-scavenging systems by gene-transfer technology has provided a powerful tool for increasing the present understanding of the potential of the defence network against oxidative damage caused by environmental stresses. Transgenic plants expressing E. coli catalase to chloroplasts with increased tolerance to oxidative stress indicate that AOS-scavenging enzymes, especially chloroplastic APX isoenzymes are sensitive under oxidative stress conditions. It is clear that a high level of endogenous ascorbate is essential effectively to maintain the antioxidant system that protects plants from oxidative damage due to biotic and abiotic stresses.

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Author and article information

Contributors

Xuchu Wang: 86-898-66987460 , xchwanghainan@163.com

Hongbin Li: 86-993-2057912 , lihb@shzu.edu.cn

Journal

Journal ID (nlm-ta): Mol Genet Genomics

Journal ID (iso-abbrev): Mol. Genet. Genomics

Title: Molecular Genetics and Genomics

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 1617-4615

ISSN (Electronic): 1617-4623

Publication date (Electronic): 6 January 2018

Publication date PMC-release: 6 January 2018

Publication date (Print): 2018

Volume: 293

Issue: 3

Pages: 685-697

Affiliations

[1 ]ISNI 0000 0001 0514 4044, GRID grid.411680.a, College of Life Sciences, Key Laboratory of Agrobiotechnology, , Shihezi University, ; Shihezi, Xinjiang China

[2 ]ISNI 0000 0000 9835 1415, GRID grid.453499.6, Institute of Tropical Biosciences and Biotechnology, , Chinese Academy of Tropical Agricultural Sciences, ; Haikou, Hainan China

Author notes

Communicated by S. Hohmann.

Article

Publisher ID: 1413

DOI: 10.1007/s00438-017-1413-2

PMC ID: 5948307

PubMed ID: 29307114

SO-VID: 630caac3-2685-4dd7-9be7-8a46e325b58c

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 2 June 2017

Date accepted : 23 December 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 31660408

Award Recipient : Hongbin Li

Funded by: Distinguished Youth innovation foundation of Bingtuan

Award ID: 2014CD003

Award Recipient : Hongbin Li

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ScienceOpen disciplines: Genetics

Keywords: ascorbate peroxidase,expression profiling,redox homeostasis,gossypium hirsutum,cotton fiber

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ScienceOpen disciplines: Genetics

Keywords: ascorbate peroxidase, expression profiling, redox homeostasis, gossypium hirsutum, cotton fiber

Genome-wide investigation and expression profiling of APX gene family in Gossypium hirsutum provide new insights in redox homeostasis maintenance during different fiber development stages

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Most cited references 38

Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.

Photosynthesis and drought: can we make metabolic connections from available data?

Regulation and function of ascorbate peroxidase isoenzymes.

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