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      Reactive oxygen species and nitric oxide induce senescence of rudimentary leaves and the expression profiles of the related genes in Litchi chinensis

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          Abstract

          Litchi is one of the most important subtropical evergreen fruit trees in southern Asia. Previous studies indicated that high-temperature conditions encourage growth of rudimentary leaves in panicles and suppress flowering. We have demonstrated that methyl viologen dichloride hydrate (MV) and sodium nitroprusside (SNP) promoted flowering in litchi partially by inhibiting the growth of rudimentary leaves via reactive oxygen species (ROS) and nitric oxide (NO). In the present study, we examined the microstructure and ultrastructure, programmed cell death (PCD) ratio, nuclei morphology of the rudimentary leaves, and the expression of senescence-related genes after the treatment with ROS or NO. The results showed that chromatins of the ROS- or NO-treated cells in the rudimentary leaves were condensed. Fusion of the cytoplasm-digesting vesicles with the vacuole and degradation of cytoplasm forming scattered debris were found in those of the treated cells. Treatment with ROS or NO increased the cell PCD ratio. Morphology of the nuclei stained by propidium iodide (PI) showed that nuclei shape became irregular after the ROS or NO treatment. Further, the expression levels of LcRboh, LcMC-1-like, and LcPirin were higher in the ROS- and NO-treated rudimentary leaves than those in the control ones, suggesting that these genes may be involved in the ROS and NO-induced senescence and abscission of the rudimentary leaves in litchi. Our results suggested that ROS and NO play an important role in inducing the senescence of the rudimentary leaves, and ROS- and NO-induced PCD may be involved in the regulation of the rudimentary leaf growth in litchi.

          Climate change: tricking the trees

          Warmer winter temperatures suppress flowering of litchi trees, threatening fruit production, but researchers have found another way to trigger litchi trees to reproduce. In litchi, spring buds contain both flower and leaf primordia, and cold cues the plants to shed the young leaves, allowing the flower primordia to develop. With recent warmer winters, the leaves are crowding out the flowers. Biyan Zhou at South China Agricultural University investigated whether spraying with compounds that make the trees produce stress-signaling molecules, such as nitrous oxide, would mimic the effects of a cold winter. Following treatment, the trees shed their rudimentary leaves and flowers developed. Microscopic examination of buds showed that the leaf shedding process looked similar to cold-triggered shedding. This study offers a method to induce litchis to flower and fruit, even in a changing climate.

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          Most cited references30

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          Dual action of the active oxygen species during plant stress responses

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            Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response.

            Nitric oxide (NO) and reactive oxygen intermediates (ROIs) play key roles in the activation of disease resistance mechanisms both in animals and plants. In animals NO cooperates with ROIs to kill tumor cells and for macrophage killing of bacteria. Such cytotoxic events occur because unregulated NO levels drive a diffusion-limited reaction with O(2)(-) to generate peroxynitrite (ONOO(-)), a mediator of cellular injury in many biological systems. Here we show that in soybean cells unregulated NO production at the onset of a pathogen-induced hypersensitive response (HR) is not sufficient to activate hypersensitive cell death. The HR is triggered only by balanced production of NO and ROIs. Moreover, hypersensitive cell death is activated after interaction of NO not with O(2)- but with H(2)O(2) generated from O(2)(-) by superoxide dismutase. Increasing the level of O(2)(-) reduces NO-mediated toxicity, and ONOO(-) is not a mediator of hypersensitive cell death. During the HR, superoxide dismutase accelerates O(2)(-) dismutation to H(2)O(2) to minimize the loss of NO by reaction with O(2)(-) and to trigger hypersensitive cell death through NO/H(2)O(2) cooperation. However, O(2)(-) rather than H(2)O(2) is the primary ROI signal for pathogen induction of glutathione S-transferase, and the rates of production and dismutation of O(2)(-) generated during the oxidative burst play a crucial role in the modulation and integration of NO/H(2)O(2) signaling in the HR. Thus although plants and animals use a similar repertoire of signals in disease resistance, ROIs and NO are deployed in strikingly different ways to trigger host cell death.
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              Morphological classification of plant cell deaths.

              Programmed cell death (PCD) is an integral part of plant development and of responses to abiotic stress or pathogens. Although the morphology of plant PCD is, in some cases, well characterised and molecular mechanisms controlling plant PCD are beginning to emerge, there is still confusion about the classification of PCD in plants. Here we suggest a classification based on morphological criteria. According to this classification, the use of the term 'apoptosis' is not justified in plants, but at least two classes of PCD can be distinguished: vacuolar cell death and necrosis. During vacuolar cell death, the cell contents are removed by a combination of autophagy-like process and release of hydrolases from collapsed lytic vacuoles. Necrosis is characterised by early rupture of the plasma membrane, shrinkage of the protoplast and absence of vacuolar cell death features. Vacuolar cell death is common during tissue and organ formation and elimination, whereas necrosis is typically found under abiotic stress. Some examples of plant PCD cannot be ascribed to either major class and are therefore classified as separate modalities. These are PCD associated with the hypersensitive response to biotrophic pathogens, which can express features of both necrosis and vacuolar cell death, PCD in starchy cereal endosperm and during self-incompatibility. The present classification is not static, but will be subject to further revision, especially when specific biochemical pathways are better defined.
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                Author and article information

                Contributors
                zhoubiyan@scau.edu.cn
                Journal
                Hortic Res
                Hortic Res
                Horticulture Research
                Nature Publishing Group UK (London )
                2052-7276
                1 May 2018
                1 May 2018
                2018
                : 5
                : 23
                Affiliations
                [1 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, College of Horticulture, , South China Agricultural University, ; Guangzhou, 510642 China
                [2 ]ISNI 0000 0004 1937 2197, GRID grid.169077.e, Department of Horticulture and Landscape Architecture, , Purdue University, ; West Lafayette, IN 47907-2010 USA
                Article
                29
                10.1038/s41438-018-0029-y
                5928110
                02db8384-49f5-46c8-b249-f5563a4ba603
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 9 August 2017
                : 26 February 2018
                : 28 February 2018
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