Salinity Stress Induces Granal Development in Bundle Sheath Chloroplasts of Maize, an NADP-Malic Enzyme-Type C<sub>4</sub>Plant

Hasan, Rusdi; Kawasaki, Michio; Taniguchi, Masaru; Miyake, Hiroshi

doi:10.1626/pps.9.256

Cited by 26 publications

(36 citation statements)

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“…4F), but the basic structural integrity was preserved. Since the low sensitivity of BSC chloroplasts and the high sensitivity of MC chloroplasts to salinity stress were previously reported in maize and several other species belonging to NADP-ME type (Hasan et al, 2005(Hasan et al, , 2006Omoto et al, 2009), this may be a common feature in all C 4 plants regardless of subtype. Hasan et al (2005) suggested that the degradation of MC chloroplasts by salinity stress in NADP-ME type species was light-dependent and associated with the generation of reactive oxygen species (ROS).…”

Section: Discussionmentioning

confidence: 70%

“…Salinity-induced granal development in BSC chloroplasts of NADP-ME type C 4 species was previously demonstrated by Hasan et al (2005Hasan et al ( , 2006 and Omoto et al (2009). However, it remains to be elucidated whether this phenomenon is general in C 4 plants, including NAD-ME and PCK type species.…”

Section: Discussionmentioning

confidence: 85%

“…In our previous study, almost all species belonging to NADP-ME type showed significant increase in these parameters under salinity (Omoto et al, 2009); however, the granal development in NAD-ME and PCK type species was not so pronounced as that in NADP-ME type species. Hasan et al (2006) suggested that the granal development in BSC chloroplasts of maize might contribute to the increase in PS activity in BSC of salt-treated plants because the photosynthetic activity in MC may be diminished due to the structural damages. Unlike NADP-ME type species, BSC chloroplasts of NAD-ME and PCK type species have inherently welldeveloped grana (Hattersley and Watson, 1992) and show PS activity as in MC chloroplasts .…”

Section: Discussionmentioning

confidence: 99%

“…In previous studies conducted from a morphological viewpoint, bundle sheath cell (BSC) chloroplasts of C 4 plants showed higher tolerance to salinity stress than mesophyll cell (MC) chloroplasts, and ultrastructure of BSC chloroplasts remained nearly unaffected by salinity even if MC chloroplasts suffered catastrophic damage (Hasan et al, 2005(Hasan et al, , 2006Barhoumi et al, 2007;Omoto et al, 2009). Meanwhile, MC chloroplasts of C 3 plants were also damaged by salinity stress as those of C 4 plants (Salama et al, 1994;Yamane et al, 2003;Fidalgo et al, 2004), in addition, MC and BSC chloroplasts were similarly affected in rice (Rahman et al, 2000).…”

mentioning

confidence: 96%

“…Hasan et al (2005Hasan et al ( , 2006 and Omoto et al (2009) demonstrated that salinity induced significant granal development in BSC chloroplasts. However, almost no work has focused on NAD-ME and PCK type C 4 species and examined how salinity affects their chloroplast structure.…”

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confidence: 99%

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Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C₄ Plants

Omoto

Taniguchi

Miyake

2010

Plant Production Science

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The effect of NaCl stress on the structure of leaf chloroplasts was investigated in several NAD-Malic enzyme (NAD-ME) and phosphoenolpyruvate carboxykinase (PCK) type C 4 plant species. Seedlings of the monocot species, except Zoysia japonica, grown in 300 mL pots were subjected to salt stress by adding 50 mL of 3% NaCl solution per day to the soil for 5 d after the fourth leaf blades were fully developed. Z. japonica and the dicot species, Amaranthus tricolor, were also treated with 3% NaCl in a similar manner from 5 wk after germination. Salt stress negatively affected the growth, chlorophyll content and chloroplast structure in all the species. At the ultrastructure level, swelling of thylakoids and disruption of envelopes were more or less observed in mesophyll cell (MC) chloroplasts after salt treatment. The structure of bundle sheath cell (BSC) chloroplasts, on the other hand, was hardly damaged under salt condition although stromal and starch areas were considerably decreased. Furthermore, salinity induced granal development in BSC chloroplasts in most species; the number of thylakoids per granum, granal indices and appressed thylakoid density in salt-treated plants were generally higher than those in control. Since the similar responses have also been reported in all NADP-ME type C 4 species investigated in our previous study, the high sensitivity to salt stress in MC chloroplasts and the granal development in BSC chloroplasts by salinity were considered to be common phenomena in all three C 4 subtypes.

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Section: Discussionmentioning

confidence: 70%

Section: Discussionmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 96%

mentioning

confidence: 99%

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Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C₄ Plants

Omoto

Taniguchi

Miyake

2010

Plant Production Science

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Significance of C4 Leaf Structure at the Tissue and Cellular Levels

Taniguchi

2018

Advances in Photosynthesis and Respiration

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Differences in photosynthetic responses of NADP-ME type C4 species to high light

Romanowska

Buczyńska

Wasilewska

et al. 2016

Planta

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Main conclusion Three species chosen as representatives of NADP-ME C4 subtype exhibit different sensitivity toward photoinhibition, and great photochemical differences were found to exist between the species. These characteristics might be due to the imbalance in the excitation energy between the photosystems present in M and BS cells, and also due to that between species caused by the penetration of light inside the leaves. Such regulation in the distribution of light intensity between M and BS cells shows that co-operation between both the metabolic systems determines effective photosynthesis and reduces the harmful effects of high light on the degradation of PSII through the production of reactive oxygen species (ROS). AbstractWe have investigated several physiological parameters of NADP-ME-type C4 species (e.g., Zea mays, Echinochloa crus-galli, and Digitaria sanguinalis) grown under moderate light intensity (200 µmol photons m−2 s−1) and, subsequently, exposed to excess light intensity (HL, 1600 µmol photons m−2 s−1). Our main interest was to understand why these species, grown under identical conditions, differ in their responses toward high light, and what is the physiological significance of these differences. Among the investigated species, Echinochloa crus-galli is best adapted to HL treatment. High resistance of the photosynthetic apparatus of E. crus-galli to HL was accompanied by an elevated level of phosphorylation of PSII proteins, and higher values of photochemical quenching, ATP/ADP ratio, activity of PSI and PSII complexes, as well as integrity of the thylakoid membranes. It was also shown that the non-radiative dissipation of energy in the studied plants was not dependent on carotenoid contents and, thus, other photoprotective mechanisms might have been engaged under HL stress conditions. The activity of the enzymes superoxide dismutase and ascorbate peroxidase as well as the content of malondialdehyde and H2O2 suggests that antioxidant defense is not responsible for the differences observed in the tolerance of NADP-ME species toward HL stress. We concluded that the chloroplasts of the examined NADP-ME species showed different sensitivity to short-term high light irradiance, suggesting a role of other factors excluding light factors, thus influencing the response of thylakoid proteins. We also observed that HL affects the mesophyll chloroplasts first hand and, subsequently, the bundle sheath chloroplasts.

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Salinity Stress Induces Granal Development in Bundle Sheath Chloroplasts of Maize, an NADP-Malic Enzyme-Type C₄Plant

Cited by 26 publications

References 37 publications

Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C₄ Plants

Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C₄ Plants

Significance of C4 Leaf Structure at the Tissue and Cellular Levels

Differences in photosynthetic responses of NADP-ME type C4 species to high light

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Salinity Stress Induces Granal Development in Bundle Sheath Chloroplasts of Maize, an NADP-Malic Enzyme-Type C4Plant

Cited by 26 publications

References 37 publications

Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C4 Plants

Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C4 Plants

Significance of C4 Leaf Structure at the Tissue and Cellular Levels

Differences in photosynthetic responses of NADP-ME type C4 species to high light

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Salinity Stress Induces Granal Development in Bundle Sheath Chloroplasts of Maize, an NADP-Malic Enzyme-Type C₄Plant

Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C₄ Plants

Effects of Salinity Stress on the Structure of Bundle Sheath and Mesophyll Chloroplasts in NAD-Malic Enzyme and PCK Type C₄ Plants