Search
2023 Volume 2
Article Contents
REVIEW   Open Access    

A review of the functions of transcription factors and related genes involved in cassava (Manihot Esculenta Crantz) response to drought stress

More Information
  • Cassava navigates drought stress via diverse mechanisms including avoidance, tolerance, resistance or recovery from effects of drought. The crop's inherent tolerance to drought stress is underpinned by a set of genes involved in several molecular pathways. Among these include transcription factors (TFs) with key roles in abscisic acid (ABA) signaling pathways. ABA is a ubiquitous phytohormone that is critical in plant growth and development processes as well as responses to abiotic stresses such as drought. This review focuses on and summarizes the current developments in the identification, characterization and functions of TFs and related genes (RGEs) implicated in ABA pathways that regulate cassava's response to drought stress. The different drought-induced experiments set up either in the field or controlled environments and omics approaches applied by researchers for gene discovery and characterization are highlighted. The roles of these drought-induced genes in other crops or plants are compared with cassava. The review reveals functions of key candidate TFs and REGs including AREBs/ABFs, NACs, bHLH, WRKY, MYC/MYB, HD-Zip, TCP, HSFs, AP2/ERFBPs, NFYA5, SLAC1, ABI1, SCaBP5, PKS3, PYR1, AP2/ERFs, DREB1A, DREB2A/B, RD29A/B, RD19, ERD1 among others. These genes are potential molecular markers that could aid in rapid introgression of drought tolerance traits not only in farmer-preferred and drought susceptible cassava genotypes, but also in other crops for improved production. Through this omics-based drought-mitigation, the negative effects of climate change could be reduced.
  • 加载中
  • [1]

    Daryanto S, Wang L, Jacinthe PA. 2017. Global synthesis of drought effects on cereal, legume, tuber and root crops production: A review. Agricultural Water Management 179:18−33

    doi: 10.1016/j.agwat.2016.04.022

    CrossRef   Google Scholar

    [2]

    Leng G, Hall J. 2019. Crop yield sensitivity of global major agricultural countries to droughts and the projected changes in the future. Science of the Total Environment 654:811−21

    doi: 10.1016/j.scitotenv.2018.10.434

    CrossRef   Google Scholar

    [3]

    Martignago D, Rico-Medina A, Blasco-Escámez D, Fontanet-Manzaneque JB, Caño-Delgado AI. 2020. Drought Resistance by Engineering Plant Tissue-Specific Responses. Frontiers in Plant Science 10:1676

    doi: 10.3389/fpls.2019.01676

    CrossRef   Google Scholar

    [4]

    Orek C, Gruissem W, Ferguson M, Vanderschuren H. 2020. Morpho-physiological and molecular evaluation of drought tolerance in cassava (Manihot esculenta Crantz). Field Crops Research 255:107861

    doi: 10.1016/j.fcr.2020.107861

    CrossRef   Google Scholar

    [5]

    Olsen KM, Schaal BA. 2001. Microsatellite variation in cassava (Manihot esculenta, Euphorbiaceae) and its wild relatives: further evidence for a southern Amazonian origin of domestication. American Journal Botany 88:131−42

    doi: 10.2307/2657133

    CrossRef   Google Scholar

    [6]

    Zhu Y, Luo X, Nawaz G, Yin J, Yang J. 2020. Physiological and Biochemical Responses of four cassava cultivars to drought stress. Scientific Reports 10:6968

    doi: 10.1038/s41598-020-63809-8

    CrossRef   Google Scholar

    [7]

    Burns A, Gleadow R, Cliff J, Zacarias A, Cavagnaro T. 2010. Cassava: The drought, war and famine crop in a changing world. Sustainability 2:3572−607

    doi: 10.3390/su2113572

    CrossRef   Google Scholar

    [8]

    Sreelakshmi K, Menon MV. 2019. Effect of moisture stress on leaf and root production in cassava (Manihot esculenta Crantz). Journal of Tropical Agriculture 57(1):40−45

    Google Scholar

    [9]

    Tize I, Fotso AK, Nukenine EN, Masso C, Ngome FA, et al. 2021. New cassava germplasm for food and nutritional security in Central Africa. Scientific Reports 11:7394

    doi: 10.1038/s41598-021-86958-w

    CrossRef   Google Scholar

    [10]

    Reincke K, Vilvert E, Fasse A, Graef F, Sieber S, Lana MA. 2018. Key factors influencing food security of smallholder farmers in Tanzania and the role of cassava as a strategic crop. Food Security 10:911−24

    doi: 10.1007/s12571-018-0814-3

    CrossRef   Google Scholar

    [11]

    Basu S, Ramegowda V, Kumar A, Pereira A. 2016. Plant adaptation to drought stress. F1000Research 5:1554

    doi: 10.12688/f1000research.7678.1

    CrossRef   Google Scholar

    [12]

    El-Sharkawy MA. 2004. Cassava biology and physiology. Plant Molecular Biology 56:481−501

    doi: 10.1007/s11103-005-2270-7

    CrossRef   Google Scholar

    [13]

    Alves AAC, Setter TL. 2000. Response of cassava to water deficit: Leaf area growth and abscisic acid. Crop Science 40:131−37

    doi: 10.2135/cropsci2000.401131x

    CrossRef   Google Scholar

    [14]

    Alves AAC, Setter TL. 2004. Abscisic acid accumulation and osmotic adjustment in cassava under water deficit. Environmental and Experimental Botany 51:259−271

    doi: 10.1016/j.envexpbot.2003.11.005

    CrossRef   Google Scholar

    [15]

    Setter TL, Fregene MA. 2007. Recent advances in molecular breeding of cassava for improved drought stress tolerance. In Advances in molecular breeding toward drought and salt tolerant crops, eds. Jenks MA, Hasegawa PM, Jain SM. Dordrecht, The Netherlands: Springer. pp. 701−11. https://doi.org/10.1007/978-1-4020-5578-2_28

    [16]

    Okogbenin E, Setter TL, Ferguson M, Mutegi R, Ceballos H, et al. 2013. Phenotypic approaches to drought in cassava: review. Frontiers in Physiology 4:00093

    doi: 10.3389/fphys.2013.00093

    CrossRef   Google Scholar

    [17]

    Li S, Yu X, Cheng Z, Yu X, Ruan M, et al. 2017. Global gene expression analysis reveals crosstalk between response mechanisms to cold and drought stresses in cassava seedlings. Frontiers in Plant Science 8:1259

    doi: 10.3389/fpls.2017.01259

    CrossRef   Google Scholar

    [18]

    Joshi R, Wani SH, Singh B, Bohra A, Dar ZA et al. 2016. Transcription factors and plants response to drought stress: Current understanding and future directions. Frontiers in Plant Science 7:1029

    doi: 10.3389/fpls.2016.01029

    CrossRef   Google Scholar

    [19]

    Fu L, Ding Z, Han B, Hu W, Li Y, et al. 2016. Physiological investigation and transcriptome analysis of polyethylene glycol (PEG)-induced dehydration stress in cassava. International Journal of Molecular Science 17:283

    doi: 10.3390/ijms17030283

    CrossRef   Google Scholar

    [20]

    Feng RJ, Ren MY, Lu LF, Peng M, Guan X, et al. 2019. Involvement of abscisic acid-responsive element-binding factors in cassava (Manihot esculenta) dehydration stress response. Scientific Reports 9:12661

    doi: 10.1038/s41598-019-49083-3

    CrossRef   Google Scholar

    [21]

    Turyagyenda LF, Kizito EB, Ferguson M, Baguma Y, Agaba M, et al. 2013. Physiological and molecular characterization of drought responses and identification of candidate tolerance genes in cassava. AoB Plants 5:plt007

    doi: 10.1093/aobpla/plt007

    CrossRef   Google Scholar

    [22]

    Gai WX, Ma X, Qiao YM, Shi BH, Haq SU, et al. 2020. Characterization of the bZIP Transcription Factor Family in Pepper (Capsicum annuum L.): CabZIP25 Positively Modulates the Salt Tolerance. Frontiers in Plant Science 11(139):00139

    doi: 10.3389/fpls.2020.00139

    CrossRef   Google Scholar

    [23]

    Fujita Y, Yoshida T, Yamaguchi-Shinozaki K. 2013. Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiologia Plantarum 147:15−27

    doi: 10.1111/j.1399-3054.2012.01635.x

    CrossRef   Google Scholar

    [24]

    Collin A, Daszkowska-Golec A, Szarejko I. 2021. Updates on the role of abscisic acid insensitive 5 (ABI5) and abscisic acid-responsive element binding factors (ABFs) in ABA signaling in different developmental stages in plants. Cells 10(8):1996

    doi: 10.3390/cells10081996

    CrossRef   Google Scholar

    [25]

    Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, et al. 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. The Plant Journal 61(4):672−685

    doi: 10.1111/j.1365-313X.2009.04092.x

    CrossRef   Google Scholar

    [26]

    Li F, Mei F, Zhang Y, Li S, Kang Z, et al. 2020. Genome-wide analysis of the AREB/ABF gene lineage in land plants and functional analysis of TaABF3 in Arabidopsis. BMC Plant Biology 20:558

    doi: 10.1186/s12870-020-02783-9

    CrossRef   Google Scholar

    [27]

    Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, et al. 2005. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiology 138:341−51

    doi: 10.1104/pp.104.059147

    CrossRef   Google Scholar

    [28]

    Hu W, Yang H, Yan Y, Wei Y, Tie W, et al. 2016. Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Scientific Reports 6:22783

    doi: 10.1038/srep22783

    CrossRef   Google Scholar

    [29]

    Fan W, Zhang M, Zhang H, Zhang P. 2012. Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS One 7:e37344

    doi: 10.1371/journal.pone.0037344

    CrossRef   Google Scholar

    [30]

    Orek CO. 2014. Morphological, physiological and molecular characterization of drought tolerance in cassava (Manihot esculenta Crantz). PhD thesis. ETH Zürich, Switzerland. www.secheresse.info/spip.php?article28679

    [31]

    Hu W, Wei Y, Xia Z, Yan Y, Hou X, et al. 2015. Genome-Wide Identification and Expression Analysis of the NAC Transcription Factor Family in Cassava. PLoS One 10(8):0136993

    doi: 10.1371/journal.pone.0136993

    CrossRef   Google Scholar

    [32]

    Li S, Zhao P, Yu X, Liao W, Peng M, et al. 2022. Cell signaling during drought and/or cold stress in cassava. Tropical Plants 1:6

    doi: 10.48130/TP-2022-0006

    CrossRef   Google Scholar

    [33]

    Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, et al. 2004. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. The Plant Journal 39:863−76

    doi: 10.1111/j.1365-313X.2004.02171.x

    CrossRef   Google Scholar

    [34]

    Li X, Chang Y, Ma S, Shen J, Hu H, et al. 2019. Genome-Wide Identification of SNAC1-Targeted Genes Involved in Drought Response in Rice. Frontiers in Plant Science 10:982

    doi: 10.3389/fpls.2019.00982

    CrossRef   Google Scholar

    [35]

    Saad AS, Li X, Li HP, Huang T, Gao CS, et al. 2013. A rice stress-responsive NAC gene enhances tolerance of transgenic wheat to drought and salt stresses. Plant Science 204:33−40

    doi: 10.1016/j.plantsci.2012.12.016

    CrossRef   Google Scholar

    [36]

    Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, et al. 2010. Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30−44

    doi: 10.1016/j.gene.2010.06.008

    CrossRef   Google Scholar

    [37]

    Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58(2):221−27

    doi: 10.1093/jxb/erl164

    CrossRef   Google Scholar

    [38]

    Phillips K, Ludidi N. 2017. Drought and exogenous abscisic acid alter hydrogen peroxide accumulation and differentially regulate the expression of two maize RD22-like genes. Scientific Reports 7:8821

    doi: 10.1038/s41598-017-08976-x

    CrossRef   Google Scholar

    [39]

    Matus JT, Aquea F, Espinoza C, Vega A, Cavallini E, et al. 2014. Inspection of the grapevine BURP superfamily highlights an expansion of RD22 genes with distinctive expression features in berry development and ABA-mediated stress responses. PLoS One 9(10):e110372

    doi: 10.1371/journal.pone.0110372

    CrossRef   Google Scholar

    [40]

    Chen T, Li W, Hu X, Guo J, Liu A, et al. 2015. A cotton MYB transcription factor, GbMYB5, is positively involved in plant adaptive response to drought stress. Plant and Cell Physiology 56(5):917−29

    doi: 10.1093/pcp/pcv019

    CrossRef   Google Scholar

    [41]

    Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, et al. 2017. RD26 mediates crosstalk between drought and brassinosteroid signaling pathways. Nature Communication 8:14573

    doi: 10.1038/ncomms14573

    CrossRef   Google Scholar

    [42]

    Wang J, Zhang L, Cao Y, Qi C, Li S, et al. 2018. CsATAF1 Positively Regulates Drought Stress Tolerance by an ABA-Dependent Pathway and by Promoting ROS Scavenging in Cucumber. Plant Cell Physiology 59(5):930−45

    doi: 10.1093/pcp/pcy030

    CrossRef   Google Scholar

    [43]

    Lokko Y, Anderson JV, Rudd S, Raji A, Horvath D, et al. 2007. Characterization of an 18, 166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes. Plant Cell Reports 26:1605−18

    doi: 10.1007/s00299-007-0378-8

    CrossRef   Google Scholar

    [44]

    Utsumi Y, Tanaka M, Morosawa T, Kurotani A, Yoshida T, et al. 2012. Transcriptome analysis using a high-density oligomicroarray under drought stress in various genotypes of cassava: An important tropical crop. DNA Research 19(4):335−45

    doi: 10.1093/dnares/dss016

    CrossRef   Google Scholar

    [45]

    Arango J, Wüst F, Beyer P, Welsch R. 2010. Characterization of phytoene synthases from cassava and their involvement in abiotic stress-mediated responses. Planta 232:1251−62

    doi: 10.1007/s00425-010-1250-6

    CrossRef   Google Scholar

    [46]

    Ding Z, Yan Y, Fu L, Meng H, Weiwei T, Wei H. 2016. Clone and expression of NAC transcription factor RD26 gene from Manihot esculenta Crantz. Journal of Southern Agriculture 47(11):1822−26

    doi: 10.3969/jissn.2095-1191.2016.11.1822

    CrossRef   Google Scholar

    [47]

    Guo J, Sun B, He H, Zhang Y, Tian H, et al. 2021. Current understanding of bHLH transcription factors in plant abiotic stress tolerance. International Journal of Molecular Science 22(9):4921

    doi: 10.3390/ijms22094921

    CrossRef   Google Scholar

    [48]

    Wang P, Wang H, Wang Y, Ren F, Liu W. 2018. Analysis of bHLH genes from foxtail millet (Setaria italica) and their potential relevance to drought stress. PLoS One 13:e0207344

    doi: 10.1371/journal.pone.0207344

    CrossRef   Google Scholar

    [49]

    Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH et al. 2011. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. The Plant Journal 65:907−21

    doi: 10.1111/j.1365-313X.2010.04477.x

    CrossRef   Google Scholar

    [50]

    Castilhos G, Lazzarotto F, Spagnolo-Fonini L, Bodanese-Zanettini MH, Margis-Pinheiro M. 2014. Possible roles of basic helix-loop-helix transcription factors in adaptation to drought. Plant Science 223:1−7

    doi: 10.1016/j.plantsci.2014.02.010

    CrossRef   Google Scholar

    [51]

    Sun X, Shantharaj D, Kang X, Ni M. 2010. Transcriptional and hormonal signaling control of Arabidopsis seed development. Current Opinion in Plant Biology 13:611−20

    doi: 10.1016/j.pbi.2010.08.009

    CrossRef   Google Scholar

    [52]

    Ling J, Jiang W, Zhang Y, Yu H, Mao Z, et al. 2011. Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics 12:471

    doi: 10.1186/1471-2164-12-471

    CrossRef   Google Scholar

    [53]

    Han M, Kim CY, Lee J, Lee SK, Jeon JS. 2014. OsWRKY42 represses OsMT1d and induces reactive oxygen species and leaf senescence in rice. Molecular Cells 37:532−39

    doi: 10.14348/molcells.2014.0128

    CrossRef   Google Scholar

    [54]

    Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, et al. 2012. WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnology Journal 10:2−11

    doi: 10.1111/j.1467-7652.2011.00634.x

    CrossRef   Google Scholar

    [55]

    Raineri J, Wang S, Peleg Z, Blumwald E, Chan RL. 2015. The rice transcription factor OsWRKY47 is a positive regulator of the response to water deficit stress. Plant Molecular Biology 88:401−13

    doi: 10.1007/s11103-015-0329-7

    CrossRef   Google Scholar

    [56]

    EI-Esawi MA, Al-Ghamdi AA, Ali HM, Ahmad M. 2019. Overexpression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in wheat (Triticum aestivum L.). Genes 10:163−76

    doi: 10.3390/genes10020163

    CrossRef   Google Scholar

    [57]

    Wei Y, Liu W, Hu W, Yan Y, Shi H. 2020. The chaperone MeHSP90 recruits MeWRKY20 and MeCatalase1 to regulate drought stress resistance in cassava. New Phytologist 226:476−91

    doi: 10.1111/nph.16346

    CrossRef   Google Scholar

    [58]

    Wei Y, Shi H, Xia Z, Tie W, Ding Z, et al. 2016. Genome-wide identification and expression analysis of the WRKY gene family in cassava. Frontiers in Plant Science 7:25

    doi: 10.3389/fpls.2016.00025

    CrossRef   Google Scholar

    [59]

    Ding Z, Tie W, Fu L, Yan Y, Liu G, et al. 2019. Strand-specific RNA-seq. based identification and functional prediction of drought-responsive lncRNAs in cassava. BMC Genomics 20:214

    doi: 10.1186/s12864-019-5585-5

    CrossRef   Google Scholar

    [60]

    Yan Y, Wang P, Lu Y, Bai Y, Wei Y, et al. 2021. MeRAV5 promotes drought stress resistance in cassava by modulating hydrogen peroxide and lignin accumulation. The Plant Journal 107:847−60

    doi: 10.1111/tpj.15350

    CrossRef   Google Scholar

    [61]

    Wang X, Niu Y, Zheng Y. 2021. Multiple functions of MYB transcription factors in abiotic stress responses. International Journal of Molecular Sciences 22(11):6125

    doi: 10.3390/ijms22116125

    CrossRef   Google Scholar

    [62]

    Ruan MB, Guo X, Wang B, Yang YL, Li WQ, et al. 2017. Genome-wide characterization and expression analysis enables identification of abiotic stress-responsive MYB transcription factors in cassava (Manihot esculenta Crantz). Journal of Experimental Botany 68:3657−72

    doi: 10.1093/jxb/erx202

    CrossRef   Google Scholar

    [63]

    Baldoni E, Genga A, Cominelli E. 2015. Plant MYB Transcription Factors: Their Role in Drought Response Mechanisms. International Journal of Molecular Sciences 16(7):15811−51

    doi: 10.3390/ijms160715811

    CrossRef   Google Scholar

    [64]

    Shin D, Moon SJ, Han S, Kim BG, Park SR, et al. 2011. Expression of StMYB1R-1, a novel potato single MYB-like domain transcription factor, increases drought tolerance. Plant Physiology 155:421−32

    doi: 10.1104/pp.110.163634

    CrossRef   Google Scholar

    [65]

    Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, et al. 1997. Role of arabidopsis MYC and MYB homologs in drought and abscisic acid-regulated gene expression. The Plant Cell 9:1859−68

    doi: 10.1105/tpc.9.10.1859

    CrossRef   Google Scholar

    [66]

    Seo PJ, Park CM. 2011. Cuticular wax biosynthesis as a way of inducing drought resistance. Plant Signaling & Behavior 6(7):1043−45

    doi: 10.4161/psb.6.7.15606

    CrossRef   Google Scholar

    [67]

    Liao W, Yang Y, Li Y, Wang G, Peng M. 2016. Genome-wide identification of cassava R2R3 MYB family genes related to abscission zone separation after environmental-stress-induced abscission. Scientific Reports 6:32006

    doi: 10.1038/srep32006

    CrossRef   Google Scholar

    [68]

    Wang B, Guo X, Zhao P, Liao W, Zeng C, et al. 2021. MeMYB26, a drought-responsive transcription factor in cassava (Manihot esculenta Crantz). Crop Breeding and Applied Biotechnology 21(1):e34432114

    doi: 10.1590/1984-70332021v21n1a4

    CrossRef   Google Scholar

    [69]

    Yang J, Ruan M, Guo X, Peng M. 2021. Characterization and functional analysis of cassava MYB transcription factor MeMYB2. Chinese Journal of Tropical Crops 42(4):936−44

    doi: 10.3969/j.issn.1000-2561.2021.04.004

    CrossRef   Google Scholar

    [70]

    Wang B, Li S, Zou L, Guo X, Liang J, et al. 2022. Natural variation MeMYB108 associated with tolerance to stress-induced leaf abscission linked to enhanced protection against reactive oxygen species in cassava. Plant Cell Reports 41:1573−1587

    doi: 10.1007/s00299-022-02879-6

    CrossRef   Google Scholar

    [71]

    Ding Z, Fu L, Yan Y, Tie W, Xia Z, Wang W, et al. 2017. Genome-wide characterization and expression profiling of HD-Zip gene family related to abiotic stress in cassava. PLoS One 12:e0173043

    doi: 10.1371/journal.pone.0173043

    CrossRef   Google Scholar

    [72]

    Söderman E, Hjellström M, Fahleson J, Engström P. 1999. The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Molecular Biology 40:1073−83

    doi: 10.1023/A:1006267013170

    CrossRef   Google Scholar

    [73]

    Johannesson H, Wang Y, Hanson J, Engström P. 2003. The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Molecular Biology 51:719−29

    doi: 10.1023/A:1022567625228

    CrossRef   Google Scholar

    [74]

    Yu X, Ruan M, Wang S, Peng M. 2014. Cloning and functional analysis of MeHDS1 from cassava in response to drought. Biotechnology Bulletin 10:76−81

    Google Scholar

    [75]

    Yu X, Guo X, Zhao P, Li S, Zou L, et al. 2023. A Homeodomain-leucine zipper I transcription factor, MeHDZ14, regulates internode elongation and leaf rolling in cassava (Manihot esculenta Crantz). The Crop Journal In press

    doi: 10.1016/j.cj.2023.03.001

    CrossRef   Google Scholar

    [76]

    Li S. 2015. The Arabidopsis thaliana TCP transcription factors: A broadening horizon beyond development. Plant Signaling & Behavior 10(7):e1044192

    doi: 10.1080/15592324.2015.1044192

    CrossRef   Google Scholar

    [77]

    Danisman S. 2016. TCP transcription factors at the interface between environmental challenges and the plant's growth responses. Frontiers in Plant Science 7:1930

    doi: 10.3389/fpls.2016.01930

    CrossRef   Google Scholar

    [78]

    Liu H, Gao Y, Wu M, Shi Y, Wang H, et al. 2020. TCP10, a TCP transcription factor in moso bamboo (Phyllostachys edulis), confers drought tolerance to transgenic plants. Environmental & Experimental Botany 172:104002

    doi: 10.1016/j.envexpbot.2020.104002

    CrossRef   Google Scholar

    [79]

    Mukhopadhyay P, Tyagi AK. 2015. OsTCP19 influences developmental and abiotic stress signaling by modulating ABI4-mediated pathways. Scientific Reports 5:9998

    doi: 10.1038/srep09998

    CrossRef   Google Scholar

    [80]

    Ding S, Cai Z, Du H, Wang H. 2019. Genome-wide analysis of TCP family genes in Zea mays L. identified a role for ZmTCP42 in drought tolerance. International Journal of Molecular Sciences 20(11):2761

    doi: 10.3390/ijms20112762

    CrossRef   Google Scholar

    [81]

    Lei N, Yu X, Li S, Zeng C, Zou L, et al. 2017. Phylogeny and expression pattern analysis of TCP transcription factors in cassava seedlings exposed to cold and/or drought stress. Scientific reports 7:10016

    doi: 10.1038/s41598-017-09398-5

    CrossRef   Google Scholar

    [82]

    Guo M, Liu JH, Ma X, Luo DX, Gong ZH, et al. 2016. The plant heat stress transcription factors (HSFs): Structure, regulation, and function in response to abiotic stresses. Frontiers in Plant Science 7:114

    doi: 10.3389/fpls.2016.00114

    CrossRef   Google Scholar

    [83]

    Ma H, Wang C, Yang B, Cheng H, Wang Z, et al. 2016. CarHSFB2, a class B heat shock transcription factor, is involved in different developmental processes and various stress responses in chickpea (Cicer arietinum L.). lant Molecular Biology Reporter 34:1−14

    doi: 10.1007/s11105-015-0892-8

    CrossRef   Google Scholar

    [84]

    Yu XY, Yao Y, Hong YH, Hou PY, Li CX, et al. 2019. Differential expression of the HSF family in cassava under biotic and abiotic stresses. Genome 62(8):563−69

    doi: 10.1139/gen-2018-0163

    CrossRef   Google Scholar

    [85]

    Zeng J, Wu C, Wang C, Liao F, Mo J, et al. 2020. Genomic analyses of heat stress transcription factors (HSFs) in simulated drought stress response and storage root deterioration after harvest in cassava. Molecular Biology Reports 47(8):5997−6007

    doi: 10.1007/s11033-020-05673-3

    CrossRef   Google Scholar

    [86]

    Li WX, Oono Y, Zhu J, He XJ, Wu JM, et al. 2008. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post-transcriptionally to promote drought resistance. The Plant Cell 20(8):2238−51

    doi: 10.1105/tpc.108.059444

    CrossRef   Google Scholar

    [87]

    Geiger D, Scherzer S, Mumm P, Stange A, Marten I, et al. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. PNAS 106(50):21425−30

    doi: 10.1073/pnas.0912021106

    CrossRef   Google Scholar

    [88]

    Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J. 2001. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. The Plant Journal 25(3):295−303

    doi: 10.1046/j.1365-313x.2001.00965.x

    CrossRef   Google Scholar

    [89]

    Lind C, Dreyer I, López-Sanjurjo EJ, von Meyer K, Ishizaki K, et al. 2015. Stomatal guard cells co-opted an ancient ABA-dependent desiccation survival system to regulate stomatal closure. Current Biology 25:928−35

    doi: 10.1016/j.cub.2015.01.067

    CrossRef   Google Scholar

    [90]

    Utsumi Y, Utsumi C, Tanaka M, Ha CV, Takahashi S, et al. 2019. Acetic Acid Treatment Enhances Drought Avoidance in Cassava (Manihot esculenta Crantz). Frontiers in Plant Science 10:521

    doi: 10.3389/fpls.2019.00521

    CrossRef   Google Scholar

    [91]

    Li X, Gao Y, Wu W, Chen L, Wang Y. 2021. Two calcium-dependent protein kinases enhance maize drought tolerance by activating anion channel ZmSLAC1 in guard cells. Plant Biotechnology Journal 20(1):143−57

    doi: 10.1111/pbi.13701

    CrossRef   Google Scholar

    [92]

    Suksamran R, Saithong T, Thammarongtham C, Kalapanulak S. 2020. Genomic and Transcriptomic Analysis Identified Novel Putative Cassava lncRNAs Involved in Cold and Drought Stress. Genes 11:366

    doi: 10.3390/genes11040366

    CrossRef   Google Scholar

    [93]

    Ruan MB, Yang YL, Li KM, Guo X, Wang B, et al. 2018. Identification and characterization of drought-responsive CC-type glutaredoxins from cassava cultivars reveals their involvement in ABA signalling. BMC Plant Biology 18:329

    doi: 10.1186/s12870-018-1528-6

    CrossRef   Google Scholar

    [94]

    Guo Y, Xiong L, Song CP, Gong D, Halfter U, et al. 2002. A Calcium Sensor and Its Interacting Protein Kinase Are Global Regulators of Abscisic Acid Signaling in Arabidopsis. Developmental Cell 3:233−44

    doi: 10.1016/S1534-5807(02)00229-0

    CrossRef   Google Scholar

    [95]

    Uraji M, Katagiri T, Okuma E, Ye W, Hossain MA, et al. 2012. Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiology 159(1):450−60

    doi: 10.1104/pp.112.195578

    CrossRef   Google Scholar

    [96]

    Peng Y, Zhang J, Cao G, Xie Y, Liu X, et al. 2010. Overexpression of a PLDα1 gene from Setaria italica enhances the sensitivity of Arabidopsis to abscisic acid and improves its drought tolerance. Plant Cell Reports 29:793−802

    doi: 10.1007/s00299-010-0865-1

    CrossRef   Google Scholar

    [97]

    Abreu FRM, Dedicova B, Vianello RP, Lanna AC, de Oliveira JAV, et al. 2018. Overexpression of a phospholipase (OsPLDα1) for drought tolerance in upland rice (Oryza sativa L.). Protoplasma 255:1751−1761

    doi: 10.1007/s00709-018-1265-6

    CrossRef   Google Scholar

    [98]

    Wang W, Feng B, Xiao J, Xia Z, Zhou X, et al. 2014. Cassava genome from a wild ancestor to cultivated varieties. Nature Communications 5:5110

    doi: 10.1038/ncomms6110

    CrossRef   Google Scholar

    [99]

    Fuchs S, Tischer SV, Wunschel C, Christmann A, Grill E. 2014. Abscisic acid sensor RCAR7/PYL13, specific regulator of protein phosphatase coreceptors. PNAS 111(15):5741−46

    doi: 10.1073/pnas.1322085111

    CrossRef   Google Scholar

    [100]

    Okamoto M, Peterson FC, Defries A, Park SY, Endo A, et al. 2013. Activation of dimeric ABA receptors elicits guard cell closure, ABA-regulated gene expression, and drought tolerance. PNAS 110(29):12132−37

    doi: 10.1073/pnas.1305919110

    CrossRef   Google Scholar

    [101]

    Tian X, Wang Z, Li X, Lv T, Liu H, et al. 2015. Characterization and functional analysis of pyrabactin resistance-like abscisic acid receptor family in rice. Rice 8:28

    doi: 10.1186/s12284-015-0061-6

    CrossRef   Google Scholar

    [102]

    Mega R, Abe F, Kim JS, Tsuboi Y, Tanaka K, et al. 2019. Tuning water-use efficiency and drought tolerance in wheat using abscisic acid receptors. Nature Plants 5:153−59

    doi: 10.1038/s41477-019-0361-8

    CrossRef   Google Scholar

    [103]

    Zhao H, Wu C, Yan Y, Tie W, Ding Z, et al. 2019. Genomic analysis of the core components of ABA signaling reveals their possible role in abiotic stress response in cassava. Environmental and Experimental Botany 167:103855

    doi: 10.1016/j.envexpbot.2019.103855

    CrossRef   Google Scholar

    [104]

    Oluwasanya DN, Gisel A, Stavolone L, Setter TL. 2021. Environmental responsiveness of flowering time in cassava genotypes and associated transcriptome changes. PLoS One 16(7):e0253555

    doi: 10.1371/journal.pone.0253555

    CrossRef   Google Scholar

    [105]

    Zeng C, Ding Z, Zhou F, Zhou Y, Yang R, et al. 2017. The discrepant and similar responses of genome-wide transcriptional profiles between drought and cold stresses in cassava. International Journal of Molecular Sciences 18:2668

    doi: 10.3390/ijms18122668

    CrossRef   Google Scholar

    [106]

    Yamada Y, Sato F. 2013. Transcription factors in Alkaloid biosynthesis. International Review of Cell and Molecular Biology 305:339−82

    doi: 10.1016/B978-0-12-407695-2.00008-1

    CrossRef   Google Scholar

    [107]

    Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2012. AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 1819:86−96

    doi: 10.1016/j.bbagrm.2011.08.004

    CrossRef   Google Scholar

    [108]

    Xu ZS, Chen M, Li LC, Ma YZ. 2011. Functions and application of the AP2/ERF transcription factor family in crop improvement. Journal of Integrative Plant Biology 53(7):570−85

    doi: 10.1111/j.1744-7909.2011.01062.x

    CrossRef   Google Scholar

    [109]

    Wang X, Han H, Yan J, Chen F, Wei W. 2015. A New AP2/ERF transcription factor from the oil plant Jatropha curcas confers salt and drought tolerance to transgenic tobacco. Applied Biochemistry Biotechnology 176:582−97

    doi: 10.1007/s12010-015-1597-z

    CrossRef   Google Scholar

    [110]

    Li Y, Zhang H, Zhang Q, Liu Q, Zhai H et al. 2019. An AP2/ERF gene, IbRAP2-12, from sweetpotato is involved in salt and drought tolerance in transgenic Arabidopsis. Plant Science 281:19−30

    doi: 10.1016/j.plantsci.2019.01.009

    CrossRef   Google Scholar

    [111]

    Gahlaut V, Jaiswal V, Kumar A, Gupta PK. 2016. Transcription factors involved in drought tolerance and their possible role in developing drought tolerant cultivars with emphasis on wheat (Triticum aestivum L). Theoretical Applied Genetics 129:2019−42

    doi: 10.1007/s00122-016-2794-z

    CrossRef   Google Scholar

    [112]

    Zhao SP, Xu ZS, Zheng WJ, Zhao W, Wang YX et al. 2017. Genome-wide analysis of the RAV family in Soybean and functional identification of GmRA-03 involvement in salt and drought stresses and exogenous ABA treatment. Frontiers in Plant Science 8:905

    doi: 10.3389/fpls.2017.00905

    CrossRef   Google Scholar

    [113]

    Zhao L, Hu Y, Chong K, Wang T. 2010. ARAG1, an ABA-responsive DREB gene, plays a role in seed germination and drought tolerance of rice. Annals of Botany 105(3):401−9

    doi: 10.1093/aob/mcp303

    CrossRef   Google Scholar

    [114]

    Shavrukov Y, Baho M, Lopato S, Langridge P. 2016. The TaDREB3 transgene transferred by conventional crossings to different genetic backgrounds of bread wheat improves drought tolerance. Plant Biotechnology Journal 14:313−22

    doi: 10.1111/pbi.12385

    CrossRef   Google Scholar

    [115]

    Todaka D, Shinozaki K, Yamaguchi-Shinozaki K. 2015. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Frontiers in Plant Science 6:84

    doi: 10.3389/fpls.2015.00084

    CrossRef   Google Scholar

    [116]

    Liao W, Li Y, Yang Y, Wang G, Peng M. 2016. Exposure to various abscission-promoting treatments suggests substantial ERF subfamily transcription factors involvement in the regulation of cassava leaf abscission. BMC Genomics 17:538

    doi: 10.1186/s12864-016-2845-5

    CrossRef   Google Scholar

    [117]

    Fan W, Hai M, Guo Y, Ding Z, Tie W, et al. 2016. The ERF transcription factor family in cassava: genome-wide characterization and expression analyses against drought stress. Scientific Reports 6:37379

    doi: 10.1038/srep37379

    CrossRef   Google Scholar

    [118]

    Ren MY, Feng RJ, Shi HR, Lu LF, Yun TY, et al. 2017. Expression patterns of members of the ethylene signaling–related gene families in response to dehydration stresses in cassava. PLoS One 12(5):e0177621

    doi: 10.1371/journal.pone.0177621

    CrossRef   Google Scholar

    [119]

    Kahraman M, Sevim G, Bor M. 2019. The Role of Proline, Glycinebetaine, and Trehalose in Stress-Responsive Gene Expression. In Osmoprotectant-Mediated Abiotic Stress Tolerance in Plants, eds. : Hossain M, Kumar V, Burritt D, Fujita M, Mäkelä P. Switzerland: Springer, Cham. pp. 241-56. https://doi.org/10.1007/978-3-030-27423-8_11

    [120]

    Koizumi M, Yamaguchi-Shinozaki K, Tsuji H, Shinozaki K. 1993. Structure and expression of two genes that encode distinct drought-inducible cysteine proteinases in Arabidopsis thaliana. Gene 129:175−82

    doi: 10.1016/0378-1119(93)90266-6

    CrossRef   Google Scholar

  • Cite this article

    Orek C. 2023. A review of the functions of transcription factors and related genes involved in cassava (Manihot Esculenta Crantz) response to drought stress. Tropical Plants 2:14 doi: 10.48130/TP-2023-0014
    Orek C. 2023. A review of the functions of transcription factors and related genes involved in cassava (Manihot Esculenta Crantz) response to drought stress. Tropical Plants 2:14 doi: 10.48130/TP-2023-0014

Figures(1)

Article Metrics

Article views(2648) PDF downloads(339)

Other Articles By Authors

REVIEW   Open Access    

A review of the functions of transcription factors and related genes involved in cassava (Manihot Esculenta Crantz) response to drought stress

Tropical Plants  2 Article number: 14  (2023)  |  Cite this article

Abstract: Cassava navigates drought stress via diverse mechanisms including avoidance, tolerance, resistance or recovery from effects of drought. The crop's inherent tolerance to drought stress is underpinned by a set of genes involved in several molecular pathways. Among these include transcription factors (TFs) with key roles in abscisic acid (ABA) signaling pathways. ABA is a ubiquitous phytohormone that is critical in plant growth and development processes as well as responses to abiotic stresses such as drought. This review focuses on and summarizes the current developments in the identification, characterization and functions of TFs and related genes (RGEs) implicated in ABA pathways that regulate cassava's response to drought stress. The different drought-induced experiments set up either in the field or controlled environments and omics approaches applied by researchers for gene discovery and characterization are highlighted. The roles of these drought-induced genes in other crops or plants are compared with cassava. The review reveals functions of key candidate TFs and REGs including AREBs/ABFs, NACs, bHLH, WRKY, MYC/MYB, HD-Zip, TCP, HSFs, AP2/ERFBPs, NFYA5, SLAC1, ABI1, SCaBP5, PKS3, PYR1, AP2/ERFs, DREB1A, DREB2A/B, RD29A/B, RD19, ERD1 among others. These genes are potential molecular markers that could aid in rapid introgression of drought tolerance traits not only in farmer-preferred and drought susceptible cassava genotypes, but also in other crops for improved production. Through this omics-based drought-mitigation, the negative effects of climate change could be reduced.

    • Global climatic changes brought on by both man-made and natural factors have resulted in general rise in temperatures and unpredictable precipitation patterns. This has increased severity and intensity of drought stress with attendant reduction in agricultural productivity. Drought stress is the most damaging abiotic stress, directly threatening food security by limiting crop growth, development, and production. Globally, drought stress has substantially affected production of major food crops causing up to 21%, 40% and more than 50% yield losses in wheat, maize and rice respectively[1]. According to future forecasts, the risk of crop loss could surpass 64%, 68%, and 70% for rice, wheat, and maize, respectively, under increasing dry conditions[2]. A critical solution is to therefore breed drought-tolerant crop varieties that can significantly improve and sustain global crop productivity to feed an ever increasing human population complexed with ongoing climatic changes. Drought tolerant crops such as cassava can sustainably produce high yield under water deficient conditions[3, 4]. Cassava is a perennial tuberous root crop of Amazonian origin[5] with a broad agro-ecological adaptability and inherent tolerance to drought stress[6]. The crop has been classified as a 'drought, war, and famine crop' in the poor world[7] due to its capacity to flourish in low fertility soils and resistance to intermittent and seasonally prolonged drought spells[8]. This has established the crop as a foundation or strategic for food security and poverty alleviation in these regions[7, 9, 10]. Generally plants either resist, avoid, escape, tolerate or recover from drought stress[11]. Plants have embedded these mechanisms at morpho-physiological, biochemical, cellular and molecular levels. Cassava is no exception. The crop deploys multiple drought response mechanisms to maintain growth and yield under water scarce conditions or periods.

      Morphological and physiological responses of cassava to drought stress has been widely researched and documented. The crop avoids drought stress by stopping leaf area expansion, reduced transpiration and by its sensitive, fast, and tight stomatal regulation over leaf gas exchange[12, 13] or general reduction in its leaf canopy that decreases transpirational surface area for water conservation[14, 15]. Further response is through decreased stomatal conductance[4], limited leaf formation and extension, increased bud dormancy and extended root growth[16]. All these responses have been directly correlated with changes in biosynthesis, accumulation and distribution of the broad-spectrum phytohormone, abscisic acid (ABA) in most if not all cassava organs and tissues. Indeed cassava varieties have accrued ABA under drought stress[14]. During abiotic stressors such as drought, ABA participates in the coordination of multiple stress signal transduction pathways or the activation of stress sensitive genes in plants. Drought stress activates the transcription factor (TFs) family of genes involved in both ABA-dependent (ABA-D) and ABA-independent (ABA-I) pathways such as the ABA responsive element binding proteins (AREBs/ABFs), Dehydration responsive element binding 2 (DREB2), MYC/MYBs and NAC (NAM, ATAF1, 2 and CUC)[17]. These TFs assist plant in tolerating abiotic stresses and other unfavorable growth conditions, thus making them viable or potential genetic candidates for widespread use in crop breeding or improvement[18]. ABA-D pathways appear to recruit antioxidant and osmoprotectant mechanisms involving glycine betaine, proline, soluble sugars among others compared to ABA-I pathways which generally involves protective proteins[13]. For cassava improvement or breeding objectives, it is important to further investigate and examine the functions of both ABA-D and ABA-I signal transduction pathways and related genes involved in increasing cassava tolerance to drought stress[4, 1921].

    • Plant growth, development, and responses to both biotic and abiotic stress are all significantly influenced by bZIP TFs[22]. AREBs/ABFs are examples of bZIP TFs that control the expression of genes that are responsive to or are dependent on ABA[23]. By binding to the conserved ABRE cis-elements in the promoter regions, AREB/ABFs exert control over the expression of target genes involved in plant response to abiotic stresses including drought, salinity, heat, oxidative and osmotic[18, 20, 24, 25]. Further, by promoting expression of several late embryogenesis genes, AREBs and ABFs promotes adaptability of different plants or crops to adverse environmental conditions[24]. For example, AREB1/ABF2, AREB2/ABF4 and ABF3 were highly induced by ABA and they both regulated ABRE-dependent ABA signaling in drought stress tolerance in Arabidopsis[25]. Additional candidate AREB/ABFs have also been over-expressed in wheat and rice under drought conditions[26, 27]. In comparison, the functions of bZIP TFs in cassava response to drought have also been studied. For instance Hu et al.[28] revealed that numerous MebZIP genes in the roots and leaves of cassava were activated by drought, indicating their participation in the plant's resistance to drought stress. In this study, eight MebZIP genes (MebZIP41, MebZIP64, MebZIP9, MebZIP58, MebZIP55, MebZIP16, MebZIP72 and MebZIP77) were up-regulated by drought stress while six (MebZIP11, MebZIP27, MebZIP52, MebZIP55, MebZIP64 and MebZIP72) were up-regulated by ABA treatment suggesting their potential role in ABA signaling. Two other MebZIP genes (MebZIP4 and MebZIP52) were over expressed under hydrogen peroxide (H2O2) treatment indicating their potential role in scavenging for reactive oxygen species (ROS) in cassava[28]. Fu et al.[19] reported five other bZIP genes (MebZIP44, MebZIP5, MebZIP53, MebZIP10 and MeHY5/TED5) involved in drought response in cassava.

      For ABFs, Feng et al.[20] reported five MeABFs (MeABF1, MeABF2, MeABF3, MeABF4 and MeABF7) that showed significantly higher expression in cassava roots and leaves as a result of drought stress. The MeABFs may activate the MeBADH1 gene by binding to its promoter region, which in turn promotes the production and accumulation of glycine betaine (GB) content in cassava[20]. Under drought, higher GB is synthesized in order to improve tissue water status and insulate biological membranes from ROS, thus osmoprotection[29]. This implied that MeABFs induced the expression of the MeBADH1 gene, which increased GB content that in turn protected the cells from dehydration by preserving osmotic balance and thus improved cassava tolerance to dehydration[20]. Fu et al.[19] also found enhanced expression of ABF2 in cassava subjected to 24-hour PEG-induced dehydration stress, while Orek[30] reported considerable up regulation of ABF2 in all cassava genotypes submitted to water deficit treatment.

    • The NAC TFs are composed of [no apical meristem (NAM)], Arabidopsis transcription activation factor [ATAF1/2] and cup-shaped cotyledon proteins [(CUC2)]. These TFs are involved in general plant growth, development as well as plant adaptability to external stimuli[31]. ABA treatment either activates or suppresses NAC TFs[32] and thus they contribute to drought resistance in plants or crops[33]. For instance, in response to drought stress, NAC genes were activated in rice[34] and wheat[35]. According to Nuruzzaman et al.[36], NAC-mediated stress responses in plants may be directly linked with ROS scavenging and plant leaf senescence. Examples of drought-inducible and ABA-mediated NAC TFs include RD22, RD26/NAC072, ATAF1, and SNAC1[33, 34, 37]. Drought stress and ABA both induced RD22, with its expression considered an ABA early response marker[38, 39]. Nine-cis-epoxycarotenoid dioxygenases (NCED) and ABA-aldehyde oxidase (AAO) are two other NAC TFs involved in ABA biosynthesis pathways[19]. The capacity to withstand drought stress has been associated with NCED3 and RD26 in cotton and transgenic tobacco[40]. RD26/NAC072 facilitates crosstalk between drought and Brassinosteroid signaling and is further involved in ABA- and JA-responsive gene expression[37, 41]. Roles of ATAF1 in drought stress and ABA response have also been reported. For example, ATAF1 positively modulated drought stress in cucumber through ABA-dependent pathway and scavenging for ROS[42]. SNAC1 is also an essential ABA signaling regulator that positively regulates the expression of a variety of ABA signaling genes[34]. Indeed ABA inducible SNAC1 in rice enhanced ABA-induced stomatal closure and improved drought resistance[31].

      Similarly, Hu et al.[31] reported expression profiles of cassava NACs TFs (MeNACs) in different cassava genotypes subjected to drought stress. For example MeNAC30 which shares high similarity with ATAF1/ANAC002 that has been shown to be involved in abiotic stress (drought and ABA) responses and leaf senescence[31]. For instance, MeNAC30 that has been reported to have high similarity to ATAF1/ANAC002, was been implicated in responses to ABA, drought and leaf senescence in cassava[31]. Upon re-watering following a drought stress treatment, MeATAF1 displayed varied expression patterns between drought tolerant and drought susceptible cassava accessions[4]. In addition, Orek et al.[4] observed distinct MeSNAC1 expression profiles in drought-tolerant and susceptible cassava cultivars and connected these to stomatal conductance. MeRD22 was also characterized by Lokko et al.[43] as one of the differentially expressed sequence tags (ESTs) with established functions in cassava drought stress responses. Further, a cassava variety that was subjected to PEG-induced dehydration stress, exhibited distinct MeRD22 expression patterns[19]. Utsumi et al.[44] reported up regulation of MeRD26 in diverse cassava genotypes under drought stress using a high-density oligomicroarray analysis.

      Diverse cassava genotypes subjected to drought stress treatment showed up-regulation of NCED3, a key gene in ABA biosynthetic pathway which encodes a member of 9-cis-epoxycarotenoid dioxygenases and MeRD26 gene that is involved in the ABA-dependent drought-induced signaling[44]. Both NCED and AAO are key enzymes involved in ABA biosynthetic pathway[19]. Similarly Orek et al.[4] showed that MeNCED3 was up-regulated in different cassava genotypes under drought and linked the gene to an ABA-dependent pathway. Furthermore, MeNCED gene was previously activated in cassava roots and was associated with high ABA levels produced in response to drought stress[45]. Ding et al.[46] reported over-expression of MeRD26 gene in cassava roots and leaves under drought stress. Fujita et al.[33] had also indicated involvement of the MeRD26 gene in drought resistance in cassava based on ABA-dependent stress signaling pathway. Fu et al.[19] showed significant activation of both MeNCED3 and MeRD26 genes in cassava genotypes under polyethylene glycol (PEG)-induced dehydration stress. MeAAO2, MeNCED7 and MeNCED8 genes were also induced in cassava under dehydration[19].

    • The bHLH TFs control a range of metabolic and developmental plant processes, including the biosynthesis of secondary metabolites, which is crucial for plant tolerance or adaptation to adverse conditions[47]. For instance, in foxtail millet and rice, bHLHs genes were induced and enhanced these plants’ tolerance to drought stress by activating the ABA and jasmonate signaling pathways, maintaining ROS homeostasis, and triggering stomatal closure[4749]. Certain bHLH TFs, including MUTE, RD29, EGLE3, GL3, and SPT, have also been linked to processes that improved drought resistance in plants, including stomatal movement, ABA synthesis, extension of root hairs, and the inhibition of leaf growth[50]. The functions of bHLH TFs in the adaptation of cassava to drought stress have also been characterized. As an illustration, the differential expression of two bHLH genes, jasmonic acid ZIM-domain protein 2/9 (JAZ2 and JAZ9), suggested that proteins associated to JA signaling transduction were involved in the response of cassava to under drought conditions[17]. Given that bHLH genes play a role in plant growth and development[51], it has been hypothesized that drought stress may preserve energy by preventing cassava growth so that it can adapt to environmental stresses[17]. Other bHLHs TFs that were identified in cassava under the dehydration stress induced by polyethylene glycol treatment included MeICE1, MebHLH4, MebHLH104, and MebHLH131-like protein[19]. These genes were either up- or down-regulated.

    • The WRKY TFs are ubiquitous in higher plants and play important roles in a variety of physiological processes and adaptation to adverse environment conditions including leaf senescence and plant response to abiotic stresses such as drought[52, 53]. WRKY TFs are important components of ABA signaling[54], and their over-expression improved drought tolerance in rice[55] and wheat[56]. Differential expression of MeWRKY genes in response to drought stress in various cassava accessions suggested that they contribute to drought stress resistance in cassava via ABA signaling and oxidative stress regulation[57, 58]. Fu et al.[19], for example, found three MeWRKY TFs (WRKY1, WRKY21, and WRKY23) that were variably expressed in response to PEG-induced dehydration stress, as well as consistent ABA-induced expression in cassava roots and leaves. Furthermore, the functional roles of MeWRKY20 and MeWRKY75 in cassava have been analyzed under drought stress[57, 59]. MeWRKY20 and MeWHY1/2/3, for example, reportedly regulated ABA accumulation in cells by inducing the expression of two ABA biosynthetic genes, MeNCED5 and MeNCED1, hence enhancing drought tolerance of wild-type cassava plants via ABA biosynthesis[32, 57, 60]. MeWRKY33, another candidate, also exhibited significant up regulation in drought-treated cassava plants[17]. Wei et al.[58] found that drought stress increased the expression of nine MeWRKY genes in the leaves and roots of different cassava accessions. These included MeWRKY6, MeWRKY11, MeWRKY14, MeWRKY18, MeWRKY20, MeWRKY40, MeWRKY42, MeWRKY49, and MeWRKY83[58]. In conclusion, cassava WRKY genes may play a key role in water intake from soil by roots, resulting in improved drought tolerance[58].

    • MYB family proteins serve a variety of roles in plant abiotic stressors such as drought, salt, and cold stress[61, 62]. They have an important role in biosynthesis of secondary metabolites like anthocyanins, flavonols, and lignin[61]. Some MYBs are specifically involved in the regulation of stomatal movement, the control of suberin and cuticular wax production, and the regulation of flower development in response to water stress[63]. Cotton, potato, and Arabidopsis MYB TFs have been shown to be involved in the adaptive response to drought stress[40, 64, 65]. The MYC (RD22BP1/AtMyc2) and MYB (AtMyb2) TFs binds to the cis-elements in the RD22 promoter and activates the RD22 gene[65]. Drought tolerance is increased by ABA-inducible MYB96, which induces stomatal closure via the RD22 gene, up-regulates cuticular wax biosynthetic enzyme genes, and modulates root growth and development[66]. Turyagyenda et al.[21] found a substantial increase in MeMYC2 expression in drought susceptible cassava genotypes compared to non-expression in drought tolerant cassava genotypes under a greenhouse water deficit treatment. In cassava, several other MYBs genes that responded to drought signals have been discovered[19, 62, 67]. For example, Liao et al.[67] found 26 cassava R2R3 MYB family genes that were expressed during water deficiency in cassava. Water deficit treatment resulted in the down regulation of MeMYB2 and MeMYB9 in cassava leaves and up regulation of MeMYB26 in cassava roots[62, 68, 69].

      The non-differential expression of MeMYB2 in cassava under PEG-induced dehydration stress suggested that the gene did not play a key part in cassava's ABA-dependent pathway[19]. However, RNAi-mediated MeMYB2 regulation increased drought tolerance in transgenic cassava[62]. Furthermore, drought stress increased the expression of MeMYB21 in cassava[17], whereas Wang et al.[68] identified MeMYB26 as a reliable candidate gene associated with cassava drought tolerance and biomass storage. In response to water deficit treatment, MYB44 and MYB60 gene regulation patterns differed between drought tolerant and drought susceptible cassava genotypes[4, 30]. Cassava exposed to PEG-induced dehydration stress showed varied expression patterns of MeMYB6, MeMYB15, and MeMYB31 in several tissues, including roots[19]. Wang et al.[70] recently found that ABA-induced induction of MeMYB108 with over-expression of gene greatly reduced the rate of drought-induced leaf abscission under drought stress in cassava. As a result, MeMYBs genes may modulate cassava responses to abiotic stress like drought through both ABA-dependent and ABA-independent mechanisms[62]. MeMYBs genes may contribute to drought stress by increasing stomatal closure in the ABA-dependent pathway.

    • The HD-Zip proteins are one of the critical TFs involved in plant growth and development through their regulatory role in the ABA signaling pathway[71]. Arabidopsis, rice, maize, soybean, legume, and banana are examples of crops or plants where HD-Zips have been studied[71]. For example Arabidopsis HD-Zip I subfamily, including AtHB5, AtHB6 and AtHB7 were either up- or down-regulated by drought stress as well as ABA treatment[72, 73]. Other research has also shown that the HD-Zip II and HD-Zip IV subfamilies also respond to drought stress and ABA treatment. Similarly, Ding et al.[71] observed differential expression patterns of multiple MeHDZ I, II, and IV subfamilies in leaves and roots of three different cassava genotypes under drought and PEG treatment. These included nine MeHDZ I subfamily (MeHDZ25, MeHDZ39, MeHDZ38, MeHDZ37, MeHDZ36, MeHDZ23, MeHDZ20, MeHDZ21, and MeHDZ26); three MeHDZ II subfamily (MeHDZ31, MeHDZ32, and MeHDZ34), and four MeHDZ IV subfamily (MeHDZ10, MeHDZ11, MeHDZ15, and MeHDZ55)[71]. Yu et al.[74] previously recorded up-regulation of MeHDS1, a member of the HD-Zip IV subfamily, in cassava during drought stress, with its expression varying more in roots than in leaves. Yu et al.[75] recently found an HD-Zip I TF, MeHDZ14, which was substantially activated by drought stress in several cassava varieties.

    • TEOSINTE BRANCHED 1 (TB1) from maize (Zea mays), CYCLOIDEA (CYC) from snapdragon (Antirrhinum majus), and PROLIFERATING CELL FACTORS 1 and 2 (PCF1 and PCF2) from rice (Oryza sativa) are the first four characterized members of the TCP family of TFs[76]. TCPs regulate a variety of biological processes throughout plant growth and development, including plant architecture, leaf morphogenesis, phytohormone pathways, and response to environmental stimuli[77]. TCP TFs control plant development and defense responses by increasing of bioactive metabolites such as brassinosteroid, jasmonate, and flavonoids[76]. TCP TFs may also play a beneficial regulatory role in plant drought tolerance via an ABA-dependent signaling pathway[78]. Drought tolerance has been improved by over-expression of TCP-TFs in bamboo[78], rice[79], and maize[80]. Similarly, the role of TCP TFs in cassava drought resistance has been studied. For example, Lei et al.[81] discovered 36 non-redundant MeTCPs in drought-stressed cassava seedlings. The drought stress treatment strongly induced seven genes (MeTCP20c, MeTCP20e, MeTCP11a, MeTCP2b, MeTCP19, MeTCP13a, and MeTCP13b)[81]. Furthermore, 22 MeTCPs were highly sensitive to ABA, showing that the MeTCPs genes may be regulated by the ABA signal pathway[81]. Furthermore, MeTCP3a and MeTC4 showed altered expression patterns under drought stress, implying that they may also play vital roles in cassava under abiotic stress conditions[81].

    • HSFs play an important role in plant stress response by regulating the expression of stress-responsive genes such as heat shock proteins (Hsps)[82]. Drought and plant hormones like ABA and ethylene have been demonstrated to influence the expression of plant HSF genes. Drought resistance in chickpea (Cicer arietinum L.), for example, was enhanced by over-expression of HSFs such as CarHSFB2[83]. The expression of HSFs genes in cassava has also been studied. Drought stress, for example, increased the transcript levels of MeHsfB3a, MeHsfA6a, MeHsfA2a, and MeHsfA9b, and additional interaction network and co-expression analyses revealed that these HSF genes may interact with Hsp70 family members to withstand environmental stresses in cassava[84]. Zeng et al.[85] discovered several MeHSFs that were up-regulated after treatments with both PEG and ABA, showing that the MeHSFs may play a role in resistance to simulated drought stress via the ABA signaling pathway. HSP90, for example, is critical for drought stress resistance in cassava by regulating ABA and hydrogen peroxide (H2O2). Among cassava's MeHSP90s, MeHSP90.9 transcript was mainly up-regulated during drought stress. MeHSP90.9 may directly activate MeWRKY20 on the W-box element of the MeNCED5 promoter, encoding a major enzyme in ABA biosynthesis and hence regulators of drought stress resistance in cassava[57]. Furthermore, MeHSP90.9 inhibited cassava leaves' ability to accumulate H2O2 during drought stress and positively regulated MeCatalase1 activity, indicating MeHSP90.9 as a possible ROS scavenger.

    • Nuclear Factor Y, Sub-unit A5 (NFYA5) are ubiquitous TFs comprised of three different sub-units (NF-YA, NF-YB, and NF-YC)[86]. NFYA5 is a member of the Arabidopsis NF-YA family whose over-expression promotes ABA-induced stomatal closure, plant survival under drought stress and by positively regulating other drought-responsive genes via the CCAAT box cis-element[86]. Indeed, Arabidopsis plants with NFYA5 over-expression showed significant drought stress resistance[86]. Similarly, in drought-stressed cassava, MeNFYA5 has been implicated in ABA-dependent signaling and stomatal movement[4, 30]. Protein kinase OST1 (open stomata 1) and protein phosphatase ABI1 (ABA insensitive 1) TFs are two critical components of the ABA signaling pathway[87]. OST1 and ABI1 are ABA transduction pathway regulators of Slow Anion Channel-Associated 1 (SLAC1)[87]. ABI1 inhibits ABA signaling, and inhibiting ABI1 could provide a strategy for increasing crop yield under drought stress[88]. Drought/ABA signaling in higher plant guard cells is mediated by the SnRK2 kinase-OST1, which activates the anion channel SLAC1[89]. Active stomatal closure necessitates the SLAC1/OST1 module[89]. OST1 encodes SnRK2, an ABA-activated protein kinase implicated in stomatal closure via ABA stimulation[90]. OST1 and SLAC1 have been associated with limiting water loss thus improving drought tolerance in maize[91]. As part of the drought avoidance strategy, transcriptomic investigation of cassava revealed that acetic acid treatment elevated the expression of ABA signaling-related genes such as MeOST1, MePP2C, and MeTSPO[90]. Drought avoidance in acetic acid-treated cassava plants was enhanced by lower stomatal conductance and transpiration rates, higher leaf relative water content, and higher levels of ABA, chlorophyll, and carotenoid[90]. Suksamran et al.[92] demonstrated that down regulation of MeSLAC1 reduces water loss in cassava during drought stress. Orek et al.[4] reported MeSLAC1 over-expression and down regulation in drought tolerant and drought susceptible cassava genotypes exposed to moisture stress. Ruan et al.[93] observed that drought stress or ABA treatment increased ABI1 expression, whereas Orek et al.[4] reported that elevated levels of MeABI1 in drought tolerant cassava genotypes was consistent with sustained stomatal opening and gradual decrease in stomatal conductance under conditions of water scarcity.

      SCaBP5, a Ca2+ binding protein, and PKS3, an interacting protein kinase, act as global modulators of ABA responses[94]. Arabidopsis mutants with suppressed SCaBP5 or PKS3 (scabp5 / pks3) had much lower transpirational water loss, rapid stomatal closure, and improved ABA response in guard cells. SCaBP5 and PKS3 are both involved in a calcium-responsive negative regulatory loop that controls ABA sensitivity[94]. Drought and ABA treatment increase the expression of SCaBP5 and PKS3. Orek et al.[4] showed increased expression of MeSCaBP5 and MePKS3 in cassava genotypes under drought and linked this with a decrease in stomatal conductance, a potential drought avoidance strategy in cassava. Phospholipase D alpha 1 (PLDα1) is a phospholipid hydrolyzing enzyme in plants that plays a role in abiotic stress responses and ABA signaling[95]. PLDα1 mediates ABA modulation of stomatal movement and its increased expression has been observed in response to dehydration and ABA treatment[96]. Elevated expression of PLDα1 improved drought tolerance in Arabidopsis[96] and upland rice[97]. Wang et al.[98] discovered PLDα1 (MesPLDα1-3) in cassava and Orek et al.[4] observed that drought stress increased the expression of MePLDα1 in drought tolerant cassava genotypes compared to its down regulation in drought susceptible genotypes. This corresponded with observed changes in stomatal conductance between the two classes of genotypes[4].

      Pyrabactin resistance 1 (PYR1) / Regulatory component of ABA receptor 11 (RCAR 11) act as ABA sensors and regulate protein phosphatase 2Cs (ABI1 and ABI2) via ABA[99]. PYR1 positively regulates ABA-mediated stomatal closure[100]. PYR1 up regulation improved drought tolerance in rice[101] and wheat[102] through positive modulation of ABA signaling. Zhao et al.[103] discovered multiple PYL/R-PP2C-SnRK2 genes that were up regulated in cassava under ABA treatment and abiotic stresses. MePYR1 was found to be involved in cassava signaling or response to ABA[104]. MeCBF3 and MeCBF4, two AP2/EREBP members that were previously linked with low temperature and ABA response, were found to be differently expressed in cassava roots during drought stress[105]. Orek et al.[4] observed increased and decreased expression of MePYR1 in drought tolerant and drought susceptible cassava genotypes respectively under drought stress treatment while Li et al.[17] analyzed a high number of 'response to ABA stimulus' genes that were significantly up- or down-regulated by drought stress in cassava, including the ABA receptor MePYL2.

    • APETALA 2/ethylene-responsive element binding factor (AP2/ERFs) is a broad set of plant-specific TFs composed of four primary subfamilies: AP2, RAV, ERF, and dehydration-responsive element-binding protein (DREBs)[106]. The AP2/EREBP stimulates the expression of abiotic stress-responsive genes by specifically binding to the DRE/CRT cis-acting element (A/GCCGAC) in their promoter regions[107]. They participate in a variety of biological processes, including growth, development, hormone and stress responses. Increased AP2/ERF expression, particularly in the DREB, ERF, and RAV subfamilies, improves drought stress tolerance, making them suitable or possible candidate genes for crop improvement or genetic engineering[108, 109]. Up-regulation of AP2/ERF TFs, for example, improved drought tolerance in rice, wheat, transgenic tobacco, and Arabidopsis by increasing photosynthesis, ABA accumulation, proline biosynthesis, and ROS scavenging[109111]. ABI3/VP1 (RAV) is another AP2/ERF-related TF that positively modulates drought tolerance in plants via ABA pathways[112]. Drought tolerance in rice[113] and wheat[114] was improved by up regulation of DREBs TFs. DREB2A and DREB2B in Arabidopsis operate as transcriptional activators in the ABA-independent (ABA-I) pathway via RD29A[ 19, 37,115]. DREB1A isolated from Arabidopsis improved drought resistance in transgenic rice[27].

      The roles of these AP2/ERF TFs in cassava drought stress response have also been documented. For example, Liao et al.[116] demonstrated that multiple AP2/ERF subfamilies play important roles in the control of ethylene- and water-deficit stress-induced leaf abscission in cassava. These included MeERF1, MeERF4, MeCRF10, MeEBE, MeESE3, MeEDF1 (RAV TF), MeRAP2.4, MeERF12, MeRAP2.6, MeCRF9, MeERF9, and MeCRF11[116]. Similarly, Fan et al.[117] discovered potential MeERFs genes that were up regulated by drought stress in cassava leaves and roots. MeERF46, MeERF56, MeERF75, MeERF35, MeERF98, MeERF133, and MeERF136 were found to be up regulated in roots, while MeERF70, MeERF17, MeERF40, MeERF116, MeERF100, and MeERF128 were found to be up regulated in leaves[117]. Ren et al.[118] related higher expression of ethylene signaling-related gene families such as MeERF6, MeERF10, MeERF11, MeERF13, MeEIL1, MeERS1 and MeERS2 with enhanced accumulation of trehalose and proline contents in cassava leaves, stems, and roots under drought stress treatment. Trehalose and proline act as compatible solutes and perform various activities in plant cells to protect them from abiotic stressors[119]. MeERF1 was similarly strongly induced in cassava by drought stress treatment[17]. Yan et al.[60] demonstrated the involvement of one cassava RAV TF candidate gene (MeRAV5) in cassava drought tolerance via H2O2 regulation and enhanced lignin buildup. MeRAV5 increased the activities of peroxidase (MePOD) and cinnamyl alcohol dehydrogenase (MeCAD15), both of which alter H2O2 and accumulation of endogenous lignin, which are significant in drought stress tolerance in cassava.

      Fu et al.[19] observed no differences in DREB2A/B gene expression levels in cassava during PEG-induced dehydration stress. However, Orek et al.[4] recorded differences in the expression of DREB1A, DREB2A/B, and RD29A/B genes in drought-tolerant and susceptible cassava genotypes exposed to different levels of water deficit treatments. Fu et al.[19] also analyzed another DREB2 member, DREB2C, which is linked in an ABA-insensitive pathway and has been shown to be co-expressed with a NAC protein, RD19, in response to dehydration and but not triggered by ABA in cassava. Under PEG-induced dehydration stress, MeRAP2.11 and MeRAP2.4 (another AP2/ERF family) for ethylene were also over expressed in cassava roots[19]. Other AP2/EREBP family members, notably MeSHN1, MeRAP2.4, MeANT, and MeABR1, have also been reported to be associated with drought stress response in cassava via hormones such as ethylene but not ABA[105].

    • Expression of cysteine proteinase RD19 is not induced by ABA, but the gene is sensitive to dehydration stress[120]. Lokko et al.[43] identified RD19 as one of the unique expressed sequence tags (ESTs) that encode proteins with known involvement in cassava drought responses. Under PEG-induced dehydration stress, up regulation of RD19 was also observed in cassava[19]. Drought, natural and dark-induced senescence, and ABA all increase the expression of ERD1, which encodes a Clp protease regulatory subunit[120]. One of the unique ESTs that encode proteins with known involvement in drought responses in cassava was Precursor to Early Response to Desiccation 1, ERD1[43]. Delta1-pyrroline-5-carboxylate synthase (P5CS), a rate-limiting enzyme in proline biosynthesis, showed consistent expression patterns with MeERD1 in cassava under drought stress, implying that MeP5CS may participate in an ABA-independent pathway in cassava via ERD1[19]. Figure 1 depicts an overview of various ABA-dependent and ABA-independent transcription factors and related genes involved in drought tolerance in cassava as reviewed above.

      Figure 1. 

      A sample of transcription factors involved in cassava response to drought stress through ABA-dependent (blue) and ABA-independent (red) molecular pathways (based on literature review for other plant species and cassava).

    • Under water deficit conditions, ABA reduces transpirational water loss from cassava leaves, promotes partial stomatal closure, reduces leaf area by restricting new leaf formation or expansion and induces leaf abscission. These morpho-physiological responses are driven by a cascade of genes or transcription factors involved in ABA signaling pathways. This review article identified candidate transcription factors within ABA pathways that could be exploited to introgress drought tolerance traits not only in susceptible cassava genotypes but also other crop species. These included genes in AREBs/ABFs, NACs, bHLH, WRKY, MYC/MYB, HD-Zip, TCP, HSFs and AP2/ERFBPs families as well as NFYA5, SLAC1, ABI1, SCaBP5, PKS3, PYR1, GRXs, AP2/ERFs, DREB1A, DREB2A/B, RD29A/B, RD19 and ERD1. They can be considered for development of molecular markers for marker-assisted selection and also candidates for genetic engineering for drought tolerance.

    • The author thanks Dr. Evans Nyaboga, department of biochemistry at the University of Nairobi for his constructive feedback.

      • The author declares that there is no conflict of interest.

      • Received 6 June 2023; Accepted 9 August 2023; Published online 4 September 2023

      • Copyright: © 2023 by the author(s). Published by Maximum Academic Press on behalf of Hainan University. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (1)  References (120)
  • About this article
    Cite this article
    Orek C. 2023. A review of the functions of transcription factors and related genes involved in cassava (Manihot Esculenta Crantz) response to drought stress. Tropical Plants 2:14 doi: 10.48130/TP-2023-0014
    Orek C. 2023. A review of the functions of transcription factors and related genes involved in cassava (Manihot Esculenta Crantz) response to drought stress. Tropical Plants 2:14 doi: 10.48130/TP-2023-0014

Catalog

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return