Salt Stress-Induced Modulation of Porphyrin Biosynthesis, Photoprotection, and Antioxidant Properties in Rice Plants (Oryza sativa)

Salt stress disrupts cellular ion homeostasis and adversely impacts plant growth and productivity. We examined the regulatory mechanisms of porphyrin biosynthesis, photoprotection, and antioxidant properties in salt-stressed rice seedlings. In response to 150 mM NaCl, the rice seedlings exhibited dehydration, reduced relative water content, and increased levels of conductivity, malondialdehyde, and H2O2. The expression levels of the salt-stress-responsive genes NHX1, SOS1, and MYB drastically increased after NaCl treatment. The seedlings grown under NaCl stress displayed declines in Fv/Fm, ΦPSII, rETRmax, and photochemical quenching but increases in nonphotochemical quenching (NPQ) and the expression of genes involved in zeaxanthin formation, BCH, and VDE. Under salt stress conditions, levels of chlorophyll precursors significantly decreased compared to controls, matching the downregulation of CHLD, CHLH, CHLI, and PORB. By contrast, NaCl treatment led to increased heme content at 24 h of treatment and significant upregulations of FC2, HO1, and HO2 compared to controls. Salt-stressed seedlings also increased their expression of CATs (catalases) and APXs (ascorbate peroxidases) as well as the activities of superoxide dismutase, CAT, APX, and peroxidase. Our results indicate that chlorophyll and heme biosynthesis involve the protective strategies for salt stress alleviation through photoprotection by the scavenging of chlorophyll precursors and NPQ as well as activating antioxidant enzymes.

[1]  V. Longo,et al.  Early Physiological, Cytological and Antioxidative Responses of the Edible Halophyte Chenopodium quinoa Exposed to Salt Stress , 2023, Antioxidants.

[2]  Sunyo Jung,et al.  Expression of the Arabidopsis Mg-chelatase H subunit alleviates iron deficiency-induced stress in transgenic rice , 2023, Frontiers in Plant Science.

[3]  B. S. Kherawat,et al.  Regulation of Reactive Oxygen Species during Salt Stress in Plants and Their Crosstalk with Other Signaling Molecules—Current Perspectives and Future Directions , 2023, Plants.

[4]  Huapeng Zhou,et al.  Plant salt response: Perception, signaling, and tolerance , 2023, Frontiers in Plant Science.

[5]  J. Minagawa,et al.  A novel method produces native LHCII aggregates from the photosynthetic membrane revealing their role in non-photochemical quenching. , 2020, The Journal of biological chemistry.

[6]  Yanxia Zhang,et al.  Salt Tolerance Mechanisms of Plants. , 2020, Annual review of plant biology.

[7]  Jiaqiang Sun,et al.  INDETERMINATE SPIKELET1 Recruits Histone Deacetylase and a Transcriptional Repression Complex to Regulate Rice Salt Tolerance1[OPEN] , 2018, Plant Physiology.

[8]  M. M. Dawuda,et al.  5-Aminolevulinic Acid (ALA) Alleviated Salinity Stress in Cucumber Seedlings by Enhancing Chlorophyll Synthesis Pathway , 2018, Front. Plant Sci..

[9]  C. Foyer,et al.  Light Signaling-Dependent Regulation of Photoinhibition and Photoprotection in Tomato1 , 2017, Plant Physiology.

[10]  T. Kleine,et al.  Salt stress-induced FERROCHELATASE 1 improves resistance to salt stress by limiting sodium accumulation in Arabidopsis thaliana , 2017, Scientific Reports.

[11]  N. Akram,et al.  Ascorbic Acid-A Potential Oxidant Scavenger and Its Role in Plant Development and Abiotic Stress Tolerance , 2017, Front. Plant Sci..

[12]  C. Foyer,et al.  Viewing oxidative stress through the lens of oxidative signalling rather than damage , 2017, The Biochemical journal.

[13]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[14]  Ai-Zhen Sun,et al.  Chloroplast Retrograde Regulation of Heat Stress Responses in Plants , 2016, Front. Plant Sci..

[15]  H. AbdElgawad,et al.  High Salinity Induces Different Oxidative Stress and Antioxidant Responses in Maize Seedlings Organs , 2016, Front. Plant Sci..

[16]  T. Phung,et al.  Alterations in the porphyrin biosynthesis and antioxidant responses to chilling and heat stresses in Oryza sativa , 2015, Biologia Plantarum.

[17]  S. Álvarez,et al.  NaCl-induced physiological and biochemical adaptative mechanisms in the ornamental Myrtus communis L. plants. , 2015, Journal of plant physiology.

[18]  N. Fernández-García,et al.  Physiological and biochemical mechanisms of the ornamental Eugenia myrtifolia L. plants for coping with NaCl stress and recovery , 2015, Planta.

[19]  Samiksha Singh,et al.  Effect of salinity stress on plants and its tolerance strategies: a review , 2015, Environmental Science and Pollution Research.

[20]  C. Foyer.  Redox homeostasis: Opening up ascorbate transport , 2015, Nature Plants.

[21]  A. Roychoudhury,et al.  Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants , 2014, Front. Environ. Sci..

[22]  T. Phung,et al.  Increased expression of Fe-chelatase leads to increased metabolic flux into heme and confers protection against photodynamically induced oxidative stress , 2014, Plant Molecular Biology.

[23]  S. Shabala,et al.  ROS homeostasis in halophytes in the context of salinity stress tolerance. , 2014, Journal of experimental botany.

[24]  E H Murchie,et al.  Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. , 2013, Journal of experimental botany.

[25]  C. Foyer,et al.  Redox signaling in plants. , 2013, Antioxidants & redox signaling.

[26]  R. Bressan,et al.  The Salt Overly Sensitive (SOS) pathway: established and emerging roles. , 2013, Molecular plant.

[27]  R. Balestrini,et al.  Ascorbate oxidase is the potential conductor of a symphony of signaling pathways , 2013, Plant signaling & behavior.

[28]  Wen‐Hao Zhang,et al.  A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice , 2012, Journal of experimental botany.

[29]  T. Phung,et al.  Porphyrin Biosynthesis Control under Water Stress: Sustained Porphyrin Status Correlates with Drought Tolerance in Transgenic Rice1[W][OA] , 2011, Plant Physiology.

[30]  Yongchao Liang,et al.  BnHO1, a haem oxygenase-1 gene from Brassica napus, is required for salinity and osmotic stress-induced lateral root formation , 2011, Journal of experimental botany.

[31]  J. Chory,et al.  Heme Synthesis by Plastid Ferrochelatase I Regulates Nuclear Gene Expression in Plants , 2011, Current Biology.

[32]  Hua Li,et al.  Expression of a Brassica napus heme oxygenase confers plant tolerance to mercury toxicity. , 2011, Plant, cell & environment.

[33]  Qing Yang,et al.  Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. , 2011, The Plant journal : for cell and molecular biology.

[34]  L. Xiong,et al.  Characterization of the β-Carotene Hydroxylase Gene DSM2 Conferring Drought and Oxidative Stress Resistance by Increasing Xanthophylls and Abscisic Acid Synthesis in Rice1[C][W][OA] , 2010, Plant Physiology.

[35]  M. Tester,et al.  Mechanisms of salinity tolerance. , 2008, Annual review of plant biology.

[36]  J. Barnes,et al.  Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggest a role for dehydroascorbate signalling. , 2008, Journal of experimental botany.

[37]  A. Ismail,et al.  Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. , 2007, Annals of botany.

[38]  R. Tanaka,et al.  Tetrapyrrole biosynthesis in higher plants. , 2007, Annual review of plant biology.

[39]  B. Grimm,et al.  Reduced activity of plastid protoporphyrinogen oxidase causes attenuated photodynamic damage during high-light compared to low-light exposure. , 2006, The Plant journal : for cell and molecular biology.

[40]  X. Hou,et al.  Promotion by 5‐Aminolevulinic Acid of Germination of Pakchoi (Brassica campestris ssp. chinensis var. communis Tsen et Lee) Seeds Under Salt Stress , 2005 .

[41]  F. Navari-Izzo,et al.  Antioxidative responses of Calendula officinalis under salinity conditions. , 2004, Plant physiology and biochemistry : PPB.

[42]  V. Mittova,et al.  Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. , 2004, Journal of experimental botany.

[43]  Jian‐Kang Zhu.  Regulation of ion homeostasis under salt stress. , 2003, Current opinion in plant biology.

[44]  F. Loreto,et al.  Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. , 2003, The New phytologist.

[45]  J. Ecker,et al.  Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX , 2003, Nature.

[46]  T. Kohchi,et al.  Expression and Biochemical Properties of a Ferredoxin-Dependent Heme Oxygenase Required for Phytochrome Chromophore Synthesis1 , 2002, Plant Physiology.

[47]  Jian-Kang Zhu,et al.  Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid , 2002, Plant Molecular Biology.

[48]  R. Mittler.  Oxidative stress, antioxidants and stress tolerance. , 2002, Trends in plant science.

[49]  K. Niyogi,et al.  Ascorbate Deficiency Can Limit Violaxanthin De-Epoxidase Activity in Vivo1 , 2002, Plant Physiology.

[50]  Jian-Kang Zhu,et al.  The Putative Plasma Membrane Na+/H+ Antiporter SOS1 Controls Long-Distance Na+ Transport in Plants Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010371. , 2002, The Plant Cell Online.

[51]  J. Papenbrock,et al.  Regulatory network of tetrapyrrole biosynthesis – studies of intracellular signalling involved in metabolic and developmental control of plastids , 2001, Planta.

[52]  P. Mullineaux,et al.  Tolerance of pea (Pisum sativum L.) to long‐term salt stress is associated with induction of antioxidant defences , 2000 .

[53]  J. Papenbrock,et al.  Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods , 1999, Planta.

[54]  A. Molina,et al.  Expression of Uroporphyrinogen Decarboxylase or Coproporphyrinogen Oxidase Antisense RNA in Tobacco Induces Pathogen Defense Responses Conferring Increased Resistance to Tobacco Mosaic Virus* , 1999, The Journal of Biological Chemistry.

[55]  David B. Collinge,et al.  Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction , 1997 .

[56]  J. Zhu,et al.  Proline Accumulation and Salt-Stress-Induced Gene Expression in a Salt-Hypersensitive Mutant of Arabidopsis , 1997, Plant physiology.

[57]  G. Paliyath,et al.  Ultraviolet-B- and Ozone-Induced Biochemical Changes in Antioxidant Enzymes of Arabidopsis thaliana , 1996, Plant physiology.

[58]  J. Varner,et al.  Hydrogen peroxide and lignification , 1993 .

[59]  K. V. Wijk,et al.  Photoinhibition of photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: Consequences for the mechanism of photoinhibition in vivo , 1993, Planta.

[60]  A. Gilmore,et al.  Zeaxanthin Formation and Energy-Dependent Fluorescence Quenching in Pea Chloroplasts under Artificially Mediated Linear and Cyclic Electron Transport. , 1991, Plant physiology.

[61]  Wolfgang Bilger,et al.  Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis , 1990, Photosynthesis Research.

[62]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[63]  S. Beale,et al.  Biosynthesis of protoheme and heme a from glutamate in maize. , 1986, Plant physiology.

[64]  T. Platt,et al.  Photosynthesis-irradiance relationships in polar and temperate phytoplankton populations , 1986, Polar Biology.

[65]  B. Halliwell,et al.  Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of Paraquat. , 1983, The Biochemical journal.

[66]  M. A. Stahmann,et al.  An improved procedure using ferricyanide for detecting catalase isozymes. , 1971, Analytical biochemistry.

[67]  Yan Guo,et al.  Elucidating the molecular mechanisms mediating plant salt-stress responses. , 2018, The New phytologist.

[68]  A. Holzwarth,et al.  The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. , 2012, Biochimica et biophysica acta.

[69]  Y. Xu,et al.  Effects of salt stress on growth , antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L . seedlings , 2005 .

[70]  W. Bilger,et al.  Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer , 2004, Photosynthesis Research.

[71]  H. Lichtenthaler.  CHLOROPHYLL AND CAROTENOIDS: PIGMENTS OF PHOTOSYNTHETIC BIOMEMBRANES , 1987 .

[72]  S. Aust,et al.  Microsomal lipid peroxidation. , 1978, Methods in enzymology.