Root and Leaf Anatomy, Ion Accumulation, and Transcriptome Pattern under Salt Stress Conditions in Contrasting Genotypes of Sorghum bicolor

Roots from salt-susceptible ICSR-56 (SS) sorghum plants display metaxylem elements with thin cell walls and large diameter. On the other hand, roots with thick, lignified cell walls in the hypodermis and endodermis were noticed in salt-tolerant CSV-15 (ST) sorghum plants. The secondary wall thickness and number of lignified cells in the hypodermis have increased with the treatment of sodium chloride stress to the plants (STN). Lignin distribution in the secondary cell wall of sclerenchymatous cells beneath the lower epidermis was higher in ST leaves compared to the SS genotype. Casparian thickenings with homogenous lignin distribution were observed in STN roots, but inhomogeneous distribution was evident in SS seedlings treated with sodium chloride (SSN). Higher accumulation of K+ and lower Na+ levels were noticed in ST compared to the SS genotype. To identify the differentially expressed genes among SS and ST genotypes, transcriptomic analysis was carried out. Both the genotypes were exposed to 200 mM sodium chloride stress for 24 h and used for analysis. We obtained 70 and 162 differentially expressed genes (DEGs) exclusive to SS and SSN and 112 and 26 DEGs exclusive to ST and STN, respectively. Kyoto Encyclopaedia of Genes and Genomes (KEGG) and Gene Ontology (GO) enrichment analysis unlocked the changes in metabolic pathways in response to salt stress. qRT-PCR was performed to validate 20 DEGs in each SSN and STN sample, which confirms the transcriptomic results. These results surmise that anatomical changes and higher K+/Na+ ratios are essential for mitigating salt stress in sorghum apart from the genes that are differentially up- and downregulated in contrasting genotypes.

[1]  Fei Zhang,et al.  Combined transcriptomic and physiological metabolomic analyses elucidate key biological pathways in the response of two sorghum genotypes to salinity stress , 2022, Frontiers in Plant Science.

[2]  S. Persson,et al.  The cell biology of primary cell walls during salt stress , 2022, The Plant cell.

[3]  Ramesh Katam,et al.  Genome-wide identification and multiple abiotic stress transcript profiling of potassium transport gene homologs in Sorghum bicolor , 2022, Frontiers in Plant Science.

[4]  S. Shabala,et al.  Unravelling the physiological basis of salinity stress tolerance in cultivated and wild rice species. , 2022, Functional plant biology : FPB.

[5]  A. Carlsbecker,et al.  Salinity induces discontinuous protoxylem via a DELLA‐dependent mechanism promoting salt tolerance in Arabidopsis seedlings , 2022, bioRxiv.

[6]  Chengxuan Chen,et al.  Comparative Transcriptome Analysis of Two Sweet Sorghum Genotypes with Different Salt Tolerance Abilities to Reveal the Mechanism of Salt Tolerance , 2022, International journal of molecular sciences.

[7]  M. R. Khan,et al.  Potassium: A track to develop salinity tolerant plants. , 2021, Plant physiology and biochemistry : PPB.

[8]  Dongping Zhang,et al.  Plant NIGT1/HRS1/HHO Transcription Factors: Key Regulators with Multiple Roles in Plant Growth, Development, and Stress Responses , 2021, International journal of molecular sciences.

[9]  Xiaopei Wang,et al.  Multiple Functions of MYB Transcription Factors in Abiotic Stress Responses , 2021, International journal of molecular sciences.

[10]  D. Yun,et al.  Microtubule Dynamics Plays a Vital Role in Plant Adaptation and Tolerance to Salt Stress , 2021, International journal of molecular sciences.

[11]  I. Qureshi,et al.  Overexpression of RNA-binding bacterial chaperones in rice lead to stay-green phenotype, improved yield and tolerance to salt and drought stresses. , 2021, Physiologia plantarum.

[12]  James F. White,et al.  Fungal endophyte Epichloë bromicola infection regulates anatomical changes to account for salt stress tolerance in wild barley (Hordeum brevisubulatum) , 2021 .

[13]  R. Dixon,et al.  Abscisic acid regulates secondary cell-wall formation and lignin deposition in Arabidopsis thaliana through phosphorylation of NST1 , 2021, Proceedings of the National Academy of Sciences.

[14]  Shamsunnaher,et al.  Rice immune sensor XA21 differentially enhances plant growth and survival under distinct levels of drought , 2020, Scientific Reports.

[15]  M. Joshi,et al.  Transcriptomic Analysis of Short-Term Salt Stress Response in Watermelon Seedlings , 2020, International journal of molecular sciences.

[16]  Ying Yu,et al.  A Na2CO3-Responsive Chitinase Gene From Leymus chinensis Improve Pathogen Resistance and Saline-Alkali Stress Tolerance in Transgenic Tobacco and Maize , 2020, Frontiers in Plant Science.

[17]  L. Barbanti,et al.  Salt Tolerance and Na Allocation in Sorghum bicolor under Variable Soil and Water Salinity , 2020, Plants.

[18]  S. Arora,et al.  Ectopic overexpression of cytosolic ascorbate peroxidase gene (Apx1) improves salinity stress tolerance in Brassica juncea by strengthening antioxidative defense mechanism , 2020, Acta Physiologiae Plantarum.

[19]  P. Suprasanna,et al.  Engineering salinity tolerance in plants: progress and prospects , 2020, Planta.

[20]  C. Ulrichs,et al.  Physiological and Anatomical Mechanisms in Wheat to Cope with Salt Stress Induced by Seawater , 2020, Plants.

[21]  J. Dinneny,et al.  A Wall with Integrity: Surveillance and Maintenance of the Plant Cell Wall Under Stress. , 2020, The New phytologist.

[22]  A. Ben-Hur,et al.  Transcriptome Analysis of Drought-Resistant and Drought-Sensitive Sorghum (Sorghum bicolor) Genotypes in Response to PEG-Induced Drought Stress , 2020, International journal of molecular sciences.

[23]  Hongwei Wang,et al.  A member of wheat class III peroxidase gene family, TaPRX-2A, enhanced the tolerance of salt stress , 2020, BMC Plant Biology.

[24]  M. O’Kennedy,et al.  Transcriptomic analysis of a Sorghum bicolor landrace identifies a role for beta-alanine betaine biosynthesis in drought tolerance , 2019 .

[25]  H. Meinke,et al.  Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice , 2019, Front. Plant Sci..

[26]  Jian Shen,et al.  The long non-coding RNA lncRNA973 is involved in cotton response to salt stress , 2019, BMC Plant Biology.

[27]  W. Tao,et al.  Arabinose biosynthesis is critical for salt stress tolerance in Arabidopsis. , 2019, The New phytologist.

[28]  S. Aliniaeifard,et al.  Calcium signaling and salt tolerance are diversely entwined in plants , 2019, Plant signaling & behavior.

[29]  K. Rajput,et al.  Immunolocalization of β-(1-4)-D-galactan, xyloglucans and xylans in the reaction xylem fibres of Leucaena leucocephala (Lam.) de Wit. , 2019, Plant physiology and biochemistry : PPB.

[30]  L. Vaahtera,et al.  Cell wall integrity maintenance during plant development and interaction with the environment , 2019, Nature Plants.

[31]  A. Hunt,et al.  Transcriptome analysis of drought-tolerant sorghum genotype SC56 in response to water stress reveals an oxidative stress defense strategy , 2019, Molecular Biology Reports.

[32]  J. Gai,et al.  Overexpression of Peroxidase Gene GsPRX9 Confers Salt Tolerance in Soybean , 2019, International journal of molecular sciences.

[33]  T. Juenger,et al.  Gene Expression analysis associated with salt stress in a reciprocally crossed rice population , 2019, Scientific Reports.

[34]  D. Yun,et al.  A Critical Role of Sodium Flux via the Plasma Membrane Na+/H+ Exchanger SOS1 in the Salt Tolerance of Rice1[OPEN] , 2019, Plant Physiology.

[35]  Shuqin Yan,et al.  Comparative transcriptome analysis of salt-sensitive and salt-tolerant maize reveals potential mechanisms to enhance salt resistance , 2019, Genes & Genomics.

[36]  Qian Zhang,et al.  Comparative Transcriptional Profiling and Physiological Responses of Two Contrasting Oat Genotypes under Salt Stress , 2018, Scientific Reports.

[37]  A. Bacic,et al.  Hitting the Wall—Sensing and Signaling Pathways Involved in Plant Cell Wall Remodeling in Response to Abiotic Stress , 2018, Plants.

[38]  Diqiu Yu,et al.  The sucrose non-fermenting-1-related protein kinases SAPK1 and SAPK2 function collaboratively as positive regulators of salt stress tolerance in rice , 2018, BMC Plant Biology.

[39]  Lifei Zhu,et al.  NtLTP4, a lipid transfer protein that enhances salt and drought stresses tolerance in Nicotiana tabacum , 2018, Scientific Reports.

[40]  T. Shah,et al.  Genome-Wide Identification and Analysis of Arabidopsis Sodium Proton Antiporter (NHX) and Human Sodium Proton Exchanger (NHE) Homologs in Sorghum bicolor , 2018, Genes.

[41]  Leonie Steinhorst,et al.  The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca2+ Signaling , 2018, Current Biology.

[42]  C. Singh,et al.  Correction: Discerning morpho-anatomical, physiological and molecular multiformity in cultivated and wild genotypes of lentil with reconciliation to salinity stress , 2017, PloS one.

[43]  N. Akhtar,et al.  Leaf anatomical and biochemical adaptations in Typha domingensis Pers. ecotypes for salinity tolerance , 2017 .

[44]  R. Lenobel,et al.  Purification of Maize Nucleotide Pyrophosphatase/Phosphodiesterase Casts Doubt on the Existence of Zeatin Cis–Trans Isomerase in Plants , 2017, Front. Plant Sci..

[45]  Rashid Al-Yahyai,et al.  The Role of Na+ and K+ Transporters in Salt Stress Adaptation in Glycophytes , 2017, Front. Physiol..

[46]  S. Shabala,et al.  Physiological and molecular mechanisms mediating xylem Na+ loading in barley in the context of salinity stress tolerance. , 2017, Plant, cell & environment.

[47]  R. O. Mesquita,et al.  Integrative Control Between Proton Pumps and SOS1 Antiporters in Roots is Crucial for Maintaining Low Na+ Accumulation and Salt Tolerance in Ammonium-Supplied Sorghum bicolor , 2017, Plant & cell physiology.

[48]  Jingjuan Yu,et al.  A Non-specific Setaria italica Lipid Transfer Protein Gene Plays a Critical Role under Abiotic Stress , 2016, Frontiers in plant science.

[49]  U. Roessner,et al.  Cell-Type-Specific H+-ATPase Activity in Root Tissues Enables K+ Retention and Mediates Acclimation of Barley (Hordeum vulgare) to Salinity Stress1[OPEN] , 2016, Plant Physiology.

[50]  S. Shabala,et al.  Difference in root K+ retention ability and reduced sensitivity of K+-permeable channels to reactive oxygen species confer differential salt tolerance in three Brassica species , 2016, Journal of experimental botany.

[51]  Jian Sun,et al.  Extracellular ATP mediates cellular K+/Na+ homeostasis in two contrasting poplar species under NaCl stress , 2016, Trees.

[52]  L. Trindade,et al.  Drought stress tolerance strategies revealed by RNA-Seq in two sorghum genotypes with contrasting WUE , 2016, BMC Plant Biology.

[53]  M. Maeshima,et al.  Contribution of PPi-Hydrolyzing Function of Vacuolar H+-Pyrophosphatase in Vegetative Growth of Arabidopsis: Evidenced by Expression of Uncoupling Mutated Enzymes , 2016, Front. Plant Sci..

[54]  L. Tran,et al.  Nitric Oxide Mitigates Salt Stress by Regulating Levels of Osmolytes and Antioxidant Enzymes in Chickpea , 2016, Front. Plant Sci..

[55]  A. Börner,et al.  Comparative proteomic analysis of β-aminobutyric acid-mediated alleviation of salt stress in barley. , 2016, Plant physiology and biochemistry : PPB.

[56]  P. Jiang,et al.  H+-pyrophosphatase from Salicornia europaea enhances tolerance to low phosphate under salinity in Arabidopsis , 2016, Plant signaling & behavior.

[57]  S. Shabala,et al.  Salt stress sensing and early signalling events in plant roots: Current knowledge and hypothesis. , 2015, Plant science : an international journal of experimental plant biology.

[58]  R. Munns,et al.  Nax loci affect SOS1-like Na+/H+ exchanger expression and activity in wheat , 2015, Journal of experimental botany.

[59]  S. Tyerman,et al.  Grapevine and Arabidopsis Cation-Chloride Cotransporters Localize to the Golgi and Trans-Golgi Network and Indirectly Influence Long-Distance Ion Transport and Plant Salt Tolerance1[OPEN] , 2015, Plant Physiology.

[60]  René Schneider,et al.  A Mechanism for Sustained Cellulose Synthesis during Salt Stress , 2015, Cell.

[61]  R. Varshney,et al.  Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. , 2015, Plant physiology and biochemistry : PPB.

[62]  Baoshan Wang,et al.  Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves , 2015, BMC Genomics.

[63]  G. Seifert,et al.  FASCICLIN LIKE ARABINOGALACTAN PROTEIN 4 and RESPIRATORY BURST OXIDASE HOMOLOG D and F independently modulate abscisic acid signaling , 2015, Plant signaling & behavior.

[64]  Xin Shen,et al.  Multiple signaling networks of extracellular ATP, hydrogen peroxide, calcium, and nitric oxide in the mediation of root ion fluxes in secretor and non-secretor mangroves under salt stress , 2014 .

[65]  Jianhua Zhang,et al.  Genome duplication improves rice root resistance to salt stress , 2014, Rice.

[66]  M. R. Hadi,et al.  The response of sweet sorghum cultivars to salt stress and accumulation of Na+, Cl- and K+ ions in relation to salinity. , 2014, Journal of environmental biology.

[67]  P. B. K. Kishor,et al.  Salt tolerance and activity of antioxidative enzymes of transgenic finger millet overexpressing a vacuolar H(+)-pyrophosphatase gene (SbVPPase) from Sorghum bicolor. , 2014, Journal of plant physiology.

[68]  M. Knight,et al.  Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress , 2014, BMC Genomics.

[69]  S. Roy,et al.  Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley , 2014, BMC Plant Biology.

[70]  S. Amaducci,et al.  Microarray analysis of differentially expressed mRNAs and miRNAs in young leaves of sorghum under dry-down conditions. , 2014, Journal of plant physiology.

[71]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[72]  F. Zeng,et al.  Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K(+) -permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley. , 2014, Plant, cell & environment.

[73]  Uzma,et al.  Genetic Improvement of Sugarcane for Drought and Salinity Stress Tolerance Using Arabidopsis Vacuolar Pyrophosphatase (AVP1) Gene , 2014, Molecular Biotechnology.

[74]  B. Liu,et al.  Identification of QTLs for salt tolerance at germination and seedling stage of Sorghum bicolor L. Moench , 2014, Euphytica.

[75]  Pradeep K. Agarwal,et al.  Bioengineering for Salinity Tolerance in Plants: State of the Art , 2013, Molecular Biotechnology.

[76]  M. Margis-Pinheiro,et al.  Heavy metal‐associated isoprenylated plant protein (HIPP): characterization of a family of proteins exclusive to plants , 2013, The FEBS journal.

[77]  Lichao Zhang,et al.  Overexpression of a wheat MYB transcription factor gene, TaMYB56-B, enhances tolerances to freezing and salt stresses in transgenic Arabidopsis. , 2012, Gene.

[78]  N. Sakthivel,et al.  Plant β-1,3-glucanases: their biological functions and transgenic expression against phytopathogenic fungi , 2012, Biotechnology Letters.

[79]  Sixue Chen,et al.  Salt stress induced proteome and transcriptome changes in sugar beet monosomic addition line M14. , 2012, Journal of plant physiology.

[80]  Andrea Polle,et al.  Salt stress induces the formation of a novel type of 'pressure wood' in two Populus species. , 2012, The New phytologist.

[81]  G. Xia,et al.  Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis , 2012, Molecular Biology Reports.

[82]  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.

[83]  Wei Li,et al.  Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. , 2012, Journal of experimental botany.

[84]  Jinxing Lin,et al.  Casparian strip development and its potential function in salt tolerance , 2011, Plant signaling & behavior.

[85]  K. Shinozaki,et al.  Generation of chimeric repressors that confer salt tolerance in Arabidopsis and rice. , 2011, Plant biotechnology journal.

[86]  B. Shiran,et al.  Evaluation of salinity tolerance in sorghum (Sorghum bicolor L.) using ion accumulation, proline and peroxidase criteria , 2011, Plant Growth Regulation.

[87]  N. Tuteja,et al.  Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. , 2010, Plant physiology and biochemistry : PPB.

[88]  E. Tavakkoli,et al.  High concentrations of Na+ and Cl– ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress , 2010, Journal of experimental botany.

[89]  C. Jang,et al.  Expressional diversity of wheat nsLTP genes: evidence of subfunctionalization via cis-regulatory divergence , 2010, Genetica.

[90]  Cole Trapnell,et al.  Role of Rodent Secondary Motor Cortex in Value-based Action Selection Nih Public Access Author Manuscript , 2006 .

[91]  T. Cuin,et al.  Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. , 2010, Plant & cell physiology.

[92]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[93]  J. Fernandes,et al.  Distinctive transcriptome responses to adverse environmental conditions in Zea mays L. , 2008, Plant biotechnology journal.

[94]  Shuangyi Zhao,et al.  A Bowman-Birk type protease inhibitor is involved in the tolerance to salt stress in wheat. , 2008, Plant, cell & environment.

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

[96]  R. Jetter,et al.  Sealing plant surfaces: cuticular wax formation by epidermal cells. , 2008, Annual review of plant biology.

[97]  E. Weiler,et al.  Adaptation to high salinity in poplar involves changes in xylem anatomy and auxin physiology. , 2006, Plant, cell & environment.

[98]  J. Davies,et al.  Extracellular Ca2+ Ameliorates NaCl-Induced K+ Loss from Arabidopsis Root and Leaf Cells by Controlling Plasma Membrane K+-Permeable Channels1 , 2006, Plant Physiology.

[99]  Z. Zheng,et al.  Molecular Characterization of the Rice Pathogenesis-related Protein, OsPR-4b, and Its Antifungal Activity Against Rhizoctonia solani , 2006 .

[100]  S. Luan,et al.  A rice quantitative trait locus for salt tolerance encodes a sodium transporter , 2005, Nature Genetics.

[101]  Viswanathan Chinnusamy,et al.  Understanding and Improving Salt Tolerance in Plants , 2005 .

[102]  C. Jang,et al.  Expression and promoter analysis of the TaLTP1 gene induced by drought and salt stress in wheat (Triticum aestivum L.) , 2004 .

[103]  J. M. Bravo,et al.  Fungus- and wound-induced accumulation of mRNA containing a class II chitinase of the pathogenesis-related protein 4 (PR-4) family of maize , 2003, Plant Molecular Biology.

[104]  G. Horgan,et al.  Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR , 2002 .

[105]  J. Zhu,et al.  Plant salt tolerance. , 2001, Trends in plant science.

[106]  S. Shabala Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll , 2000 .

[107]  A. Blum,et al.  Yield and Yield Stability of Four Population Types of Grain Sorghum in a Semi‐Arid Area of Kenya , 2000, Crop Science.

[108]  M. Delseny,et al.  Characterization of a gene encoding an abscisic acid‐inducible type‐2 lipid transfer protein from rice , 1998, FEBS letters.

[109]  F M Poulsen,et al.  Primary structure of barwin: a barley seed protein closely related to the C-terminal domain of proteins encoded by wound-induced plant genes. , 1992, Biochemistry.

[110]  R. Leah,et al.  Biochemical and molecular characterization of three barley seed proteins with antifungal properties. , 1991, The Journal of biological chemistry.

[111]  G. Berlyn,et al.  Botanical Microtechnique and Cytochemistry , 1991 .

[112]  Y. Kalra,et al.  Chloride determination and levels in the soil-plant environment , 1981 .

[113]  E. Reynolds THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.

[114]  Singh Alka,et al.  Salt Tolerance of Sorghum bicolor Cultivars during Germination and Seedling Growth , 2012 .

[115]  Ute Baumann,et al.  Root-specific transcript profiling of contrasting rice genotypes in response to salinity stress. , 2011, Molecular plant.

[116]  Iqra,et al.  Induction of salt tolerance in two cultivars of sorghum (Sorghum bicolor L.) by exogenous application of proline at seedling stage. , 2010 .

[117]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[118]  R. Bressan,et al.  Isolation and characterisation of wheat cDNA clones encoding PR4 proteins. , 1999, DNA sequence : the journal of DNA sequencing and mapping.

[119]  L. Donaldson Lignin Distribution During Latewood Formation in Pinus Radiata D. Don , 1992 .