Transcriptomic analysis reveals mechanisms for the different drought tolerance of sweet potatoes

Drought is a common environmental stress with great negative impacts on plant growth, development and geographical distribution as well as agriculture and food production. Sweet potato is characterized by starchy, fresh and pigmented tuber, and is regarded as the seventh most important food crop. However, there has been no comprehensive study of the drought tolerance mechanism of different sweet potato cultivars to date. Here, we studied the mechanism for drought response of seven sweet potato drought-tolerant cultivars using the drought coefficients, physiological indicators and transcriptome sequencing. The seven sweet potato cultivars were classified into four groups of drought tolerance performance. A large number of new genes and transcripts were identified, with an average of about 8000 new genes per sample. Alternative splicing events in sweet potato, which were dominated by first exon and last exon alternative splicing, were not conserved among different cultivars and not significantly affected by drought stress. Furthermore, different drought-tolerance mechanisms were revealed through differentially expressed gene analysis and functional annotation. Two drought-sensitive cultivars, Shangshu-9 and Xushu-22, mainly resisted drought stress by up-regulating plant signal transduction. The other drought-sensitive cultivar Jishu-26 responded to drought stress by down-regulating isoquinoline alkaloid biosynthesis and nitrogen/carbohydrate metabolism. In addition, the drought-tolerant cultivar Chaoshu-1 and drought-preferred cultivar Z15-1 only shared 9% of differentially expressed genes, as well as many opposite metabolic pathways in response to drought. They mainly regulated flavonoid and carbohydrate biosynthesis/metabolism in response to drought, while Z15-1 increased photosynthesis and carbon fixation capacity. The other drought-tolerant cultivar Xushu-18 responded to drought stress by regulating the isoquinoline alkaloid biosynthesis and nitrogen/carbohydrate metabolism. The extremely drought-tolerant cultivar Xuzi-8 was almost unaffected by drought stress and responded to drought environment only by regulating the cell wall. These findings provide important information for the selection of sweet potatoes for specific purposes.

[1]  Lingxiao Zhao,et al.  Metabolomic and Transcriptomic Analyses of the Flavonoid Biosynthetic Pathway for the Accumulation of Anthocyanins and Other Flavonoids in Sweetpotato Root Skin and Leaf Vein Base. , 2022, Journal of agricultural and food chemistry.

[2]  Jianhua Zhu,et al.  Abiotic stress responses in plants , 2021, Nature Reviews Genetics.

[3]  R. Ohmura,et al.  Changes in polyphenols, anthocyanins, and DPPH radical-scavenging activities in sweetpotato (Ipomoea batatas L.) during tuber growth , 2021 .

[4]  Zhen Qin,et al.  不同抗旱性甘薯品种叶片生理性状差异及抗旱指标筛选 , 2021, ACTA AGRONOMICA SINICA.

[5]  Baocun Zhao,et al.  OsIAA20, an Aux/IAA protein, mediates abiotic stress tolerance in rice through an ABA pathway. , 2021, Plant science : an international journal of experimental plant biology.

[6]  Ting Peng,et al.  Transcriptome analysis of Chongyi wild mandarin, a wild species more cold-tolerant than Poncirus trifoliata, reveals key pathways in response to cold , 2021 .

[7]  S. Ceccarelli,et al.  In pursuit of a better world: crop improvement and the CGIAR , 2021, Journal of experimental botany.

[8]  H. Nguyen,et al.  Analysis of Whole Transcriptome RNA-seq Data Reveals Many Alternative Splicing Events in Soybean Roots under Drought Stress Conditions , 2020, Genes.

[9]  Tao Xu,et al.  Drought-Induced Responses of Nitrogen Metabolism in Ipomoea batatas , 2020, Plants.

[10]  Wei Tang,et al.  RNA-sequencing analysis revealed genes associated drought stress responses of different durations in hexaploid sweet potato , 2020, Scientific Reports.

[11]  T. Ault.  On the essentials of drought in a changing climate , 2020, Science.

[12]  Fan Liang,et al.  A global survey of the transcriptome of the allopolyploid Brassica napus based on single molecule long-read isoform sequencing and Illumina-based RNA-seq data. , 2020, The Plant journal : for cell and molecular biology.

[13]  W. Cho,et al.  Sweet potato viromes in eight different geographical regions in Korea and two different cultivars , 2020, Scientific Reports.

[14]  S. Kwak,et al.  Comparative transcriptome profiling of tuberous roots of two sweetpotato lines with contrasting low temperature tolerance during storage. , 2019, Gene.

[15]  N. Basílio,et al.  Purple-fleshed sweet potato acylated anthocyanins: Equilibrium network and photophysical properties. , 2019, Food chemistry.

[16]  Jeung Joo Lee,et al.  Transcriptomic changes in sweetpotato peroxidases in response to infection with the root-knot nematode Meloidogyne incognita , 2019, Molecular Biology Reports.

[17]  S. Kwak,et al.  De novo transcriptome sequencing and gene expression profiling of sweet potato leaves during low temperature stress and recovery. , 2019, Gene.

[18]  J. Ecker,et al.  Auxin-sensitive Aux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels , 2019, Nature Communications.

[19]  H. Zhai,et al.  Transcriptome profiling reveals insights into the molecular mechanism of drought tolerance in sweetpotato , 2019, Journal of Integrative Agriculture.

[20]  Min-Yao Jhu,et al.  MicroR408 regulates defense response upon wounding in sweet potato , 2018, Journal of experimental botany.

[21]  Z. Fei,et al.  Transcriptomic analysis of sweet potato under dehydration stress identifies candidate genes for drought tolerance , 2018, Plant direct.

[22]  Sung Chul Lee,et al.  A DEAD-box RNA helicase, RH8, is critical for regulation of ABA signalling and the drought stress response via inhibition of PP2CA activity. , 2018, Plant, cell & environment.

[23]  Mingming Xin,et al.  Global profiling of alternative splicing landscape responsive to drought, heat and their combination in wheat (Triticum aestivum L.) , 2017, Plant biotechnology journal.

[24]  Maojun Wang,et al.  A global survey of alternative splicing in allopolyploid cotton: landscape, complexity and regulation. , 2018, The New phytologist.

[25]  R. Mittler,et al.  Plant adaptations to the combination of drought and high temperatures. , 2018, Physiologia plantarum.

[26]  Ming Yan,et al.  Alternative splicing complexity contributes to genetic improvement of drought resistance in the rice maintainer HuHan2B , 2017, Scientific Reports.

[27]  Martin Vingron,et al.  Haplotype-resolved sweet potato genome traces back its hexaploidization history , 2017, Nature Plants.

[28]  Zhongchi Liu,et al.  Global identification of alternative splicing via comparative analysis of SMRT‐ and Illumina‐based RNA‐seq in strawberry , 2017, The Plant journal : for cell and molecular biology.

[29]  J. Palta,et al.  Review: An integrated framework for crop adaptation to dry environments: Responses to transient and terminal drought. , 2016, Plant science : an international journal of experimental plant biology.

[30]  Tao Xu,et al.  NaCl-induced changes of ion homeostasis and nitrogen metabolism in two sweet potato (Ipomoea batatas L.) cultivars exhibit different salt tolerance at adventitious root stage , 2016 .

[31]  Tyson A. Clark,et al.  Unveiling the complexity of the maize transcriptome by single-molecule long-read sequencing , 2016, Nature Communications.

[32]  Jun Tang,et al.  Transcriptome Sequencing of the Sweet Potato Progenitor (Ipomoea Trifida (H.B.K.) G. Don.) and Discovery of Drought Tolerance Genes , 2016, Tropical Plant Biology.

[33]  Jukon Kim,et al.  OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. , 2015, Plant science : an international journal of experimental plant biology.

[34]  G. C. Yencho,et al.  Screening sweetpotato genotypes for tolerance to drought stress , 2015 .

[35]  M. Beatty,et al.  Genome-Wide Analysis of Alternative Splicing in Zea mays: Landscape and Genetic Regulation[C][W] , 2014, Plant Cell.

[36]  K. Shinozaki,et al.  The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat , 2014, Front. Plant Sci..

[37]  C. N. Stewart,et al.  High-throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. , 2014, Plant biotechnology journal.

[38]  K. R. Reddy,et al.  Growth, developmental, and physiological responses of two sweetpotato (Ipomoea batatas L. [Lam]) cultivars to early season soil moisture deficit , 2014 .

[39]  M. Laing,et al.  Self- and cross-incompatibilities in sweetpotato and their implications on breeding , 2013 .

[40]  X. Tao,et al.  Transcriptome Analysis to Identify Putative Floral-Specific Genes and Flowering Regulatory-Related Genes of Sweet Potato , 2013, Bioscience, biotechnology, and biochemistry.

[41]  S. Salzberg,et al.  Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues , 2013, F1000Research.

[42]  John W. S. Brown,et al.  Alternative Splicing at the Intersection of Biological Timing, Development, and Stress Responses[OPEN] , 2013, Plant Cell.

[43]  S. Eddy,et al.  Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions , 2013, Nucleic acids research.

[44]  D. McKey,et al.  On the origin of sweet potato (Ipomoea batatas (L.) Lam.) genetic diversity in New Guinea, a secondary centre of diversity , 2013, Heredity.

[45]  M. Kalita,et al.  Molecular cloning, expression and computational analysis of a water stress inducible copper-containing amine oxidase gene (CuAO) from tea plant [ Camellia sinensis (L.) O. Kuntze] , 2012 .

[46]  M. Yarnia,et al.  Evaluation of drought tolerance indices among some winter rapeseed cultivars , 2011 .

[47]  Xinliang Chen,et al.  De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweetpotato (Ipomoea batatas) , 2010, BMC Genomics.

[48]  Ming Chen,et al.  Auxin-related gene families in abiotic stress response in Sorghum bicolor , 2010, Functional & Integrative Genomics.

[49]  Cha Young Kim,et al.  Exogenous sucrose utilization and starch biosynthesis among sweet potato cultivars. , 2010, Carbohydrate research.

[50]  Xuegong Zhang,et al.  DEGseq: an R package for identifying differentially expressed genes from RNA-seq data , 2010, Bioinform..

[51]  K. Shinozaki,et al.  Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes , 2010, Molecular Genetics and Genomics.

[52]  S. Takumi,et al.  Allopolyploidization reduces alternative splicing efficiency for transcripts of the wheat DREB2 homolog, WDREB2. , 2009, Genome.

[53]  P. J. Andralojc,et al.  Arabidopsis sucrose non-fermenting-1-related protein kinase-1 and calcium-dependent protein kinase phosphorylate conserved target sites in ABA response element binding proteins , 2008 .

[54]  M. Robles,et al.  University of Birmingham High throughput functional annotation and data mining with the Blast2GO suite , 2022 .

[55]  K. Shinozaki,et al.  Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. , 2007, The Plant journal : for cell and molecular biology.

[56]  V. Brendel,et al.  Genomewide comparative analysis of alternative splicing in plants. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Tao Cai,et al.  Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary , 2005, Bioinform..

[58]  Donald R. Davis,et al.  Changes in USDA Food Composition Data for 43 Garden Crops, 1950 to 1999 , 2004, Journal of the American College of Nutrition.

[59]  I. D. Teare,et al.  Rapid determination of free proline for water-stress studies , 1973, Plant and Soil.

[60]  Susumu Goto,et al.  The KEGG resource for deciphering the genome , 2004, Nucleic Acids Res..

[61]  W. Van Camp,et al.  Oxidative stress, heat shock and drought differentially affect expression of a tobacco protein phosphatase 2C. , 2000, Journal of experimental botany.

[62]  Michael Y. Galperin,et al.  The COG database: a tool for genome-scale analysis of protein functions and evolution , 2000, Nucleic Acids Res..

[63]  W. Schapaugh,et al.  Stress Tolerance in Soybeans. I. Evaluation of Three Screening Techniques for Heat and Drought Tolerance 1 , 1984 .