CLC number:
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 2023-12-12
Cited: 0
Clicked: 1748
Sakura KARUNARATHNE, Esther WALKER, Darshan SHARMA, Chengdao LI, Yong HAN. Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance[J]. Journal of Zhejiang University Science B, 2023, 24(12): 1069-1092.
@article{title="Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance",
author="Sakura KARUNARATHNE, Esther WALKER, Darshan SHARMA, Chengdao LI, Yong HAN",
journal="Journal of Zhejiang University Science B",
volume="24",
number="12",
pages="1069-1092",
year="2023",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2200552"
}
%0 Journal Article
%T Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance
%A Sakura KARUNARATHNE
%A Esther WALKER
%A Darshan SHARMA
%A Chengdao LI
%A Yong HAN
%J Journal of Zhejiang University SCIENCE B
%V 24
%N 12
%P 1069-1092
%@ 1673-1581
%D 2023
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2200552
TY - JOUR
T1 - Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance
A1 - Sakura KARUNARATHNE
A1 - Esther WALKER
A1 - Darshan SHARMA
A1 - Chengdao LI
A1 - Yong HAN
J0 - Journal of Zhejiang University Science B
VL - 24
IS - 12
SP - 1069
EP - 1092
%@ 1673-1581
Y1 - 2023
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2200552
Abstract: Abiotic stresses, predominately drought, heat, salinity, cold, and waterlogging, adversely affect cereal crops. They limit barley production worldwide and cause huge economic losses. In barley, functional genes under various stresses have been identified over the years and genetic improvement to stress tolerance has taken a new turn with the introduction of modern gene-editing platforms. In particular, clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) is a robust and versatile tool for precise mutation creation and trait improvement. In this review, we highlight the stress-affected regions and the corresponding economic losses among the main barley producers. We collate about 150 key genes associated with stress tolerance and combine them into a single physical map for potential breeding practices. We also overview the applications of precise base editing, prime editing, and multiplexing technologies for targeted trait modification, and discuss current challenges including high-throughput mutant genotyping and genotype dependency in genetic transformation to promote commercial breeding. The listed genes counteract key stresses such as drought, salinity, and nutrient deficiency, and the potential application of the respective gene-editing technologies will provide insight into barley improvement for climate resilience.
[1]AbassM, MorrisPC, 2013. The Hordeum vulgare signalling protein MAP kinase 4 is a regulator of biotic and abiotic stress responses. J Plant Physiol, 170(15):1353-1359.
[2]AcostaJA, FazA, JansenB, et al., 2011. Assessment of salinity status in intensively cultivated soils under semiarid climate, Murcia, SE Spain. J Arid Environ, 75(11):1056-1066.
[3]AdisaOM, MasindeM, BotaiJO, et al., 2020. Bibliometric analysis of methods and tools for drought monitoring and prediction in Africa. Sustainability, 12(16):6516.
[4]AfganE, BakerD, BatutB, et al., 2018. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res, 46(W1):W537-W544.
[5]AhmadalipourA, MoradkhaniH, CastellettiA, et al., 2019. Future drought risk in Africa: integrating vulnerability, climate change, and population growth. Sci Total Environ, 662:672-686.
[6]AhmedF, RafiiMY, IsmailMR, et al., 2013. Waterlogging tolerance of crops: breeding, mechanism of tolerance, molecular approaches, and future prospects. Biomed Res Int, 2013:963525.
[7]al AbdallatAM, AyadJY, abu EleneinJM, et al., 2014. Overexpression of the transcription factor HvSNAC1 improves drought tolerance in barley (Hordeum vulgare L.). Mol Breeding, 33(2):401-414.
[8]AlexanderRD, Wendelboe-NelsonC, MorrisPC, 2019. The barley transcription factor HvMYB1 is a positive regulator of drought tolerance. Plant Physiol Biochem, 142:246-253.
[9]AlghuthaymiMA, AhmadA, KhanZ, et al., 2021. Exosome/liposome-like nanoparticles: new carriers for CRISPR genome editing in plants. Int J Mol Sci, 22(14):7456.
[10]AliQ, MalikA, 2021. Genetic response of growth phases for abiotic environmental stress tolerance in cereal crop plants. Genetika, 53(1):419-456.
[11]AmanR, AliZ, ButtH, et al., 2018. RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol, 19:1.
[12]AnYH, GuZ, JiaoXY, et al., 2022. Enhanced N2O emissions from winter wheat field induced by winter irrigation in the North China Plain. Agronomy, 12(4):955.
[13]AnzaloneAV, RandolphPB, DavisJR, et al., 2019. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature, 576(7785):149-157.
[14]Araneda-CabreraRJ, BermúdezM, PuertasJ, 2021. Benchmarking of drought and climate indices for agricultural drought monitoring in Argentina. Sci Total Environ, 790:148090.
[15]AtkinsonNJ, UrwinPE, 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot, 63(10):3523-3543.
[16]BahraniHA, GhazviniH, AmiriB, et al., 2023. Responses of barley (Hordeum vulgare L.) genotypes to salinity stress under controlled and field conditions. Gesunde Pflanz, 75:499-513.
[17]BennettA, 2021. A Review of the Economics of Regenerative Agriculture in Western Australia. Department of Primary Industries and Regional Development, Western Australian Government, Perth, Australia. https://library.dpird.wa.gov.au/pubns/153
[18]BentoVA, RibeiroAFS, RussoA, et al., 2021. The impact of climate change in wheat and barley yields in the Iberian Peninsula. Sci Rep, 11:15484.
[19]BillonP, BryantEE, JosephSA, et al., 2017. CRISPR-mediated base editing enables efficient disruption of eukaryotic genes through induction of STOP codons. Mol Cell, 67(6):1068-1079.e4.
[20]Borrego-BenjumeaA, CarterA, GlennAJ, et al., 2019. Impact of excess moisture due to precipitation on barley grain yield in the Canadian Prairies. Can J Plant Sci, 99(1):93-96.
[21]Borrego-BenjumeaA, CarterA, TuckerJR, et al., 2020. Genome-wide analysis of gene expression provides new insights into waterlogging responses in barley (Hordeum vulgare L.). Plants (Basel), 9(2):240.
[22]BorychowskiM, GrzelakA, PopławskiŁ, 2022. What drives low-carbon agriculture? The experience of farms from the Wielkopolska region in Poland. Environ Sci Pollut Res, 29(13):18641-18652.
[23]BoselloF, NichollsRJ, RichardsJ, et al., 2012. Economic impacts of climate change in Europe: sea-level rise. Climatic Change, 112(1):63-81.
[24]BrinkmanEK, ChenT, AmendolaM, et al., 2014. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res, 42(22):e168.
[25]BrissonN, RebièreB, ZimmerD, et al., 2002. Response of the root system of a winter wheat crop to waterlogging. Plant Soil, 243(1):43-55.
[26]ButtH, RaoGS, SedeekK, et al., 2020. Engineering herbicide resistance via prime editing in rice. Plant Biotechnol J, 18(12):2370-2372.
[27]CammaranoD, CeccarelliS, GrandoS, et al., 2019. The impact of climate change on barley yield in the Mediterranean basin. Eur J Agron, 106:1-11.
[28]ChallinorAJ, WatsonJ, LobellDB, et al., 2014. A meta-analysis of crop yield under climate change and adaptation. Nat Climate Change, 4(4):287-291.
[29]ChatzidimopoulosM, GanopoulosI, Moraitou-DapontaE, et al., 2019. High-resolution melting (HRM) analysis reveals genotypic differentiation of Venturia inaequalis populations in Greece. Front Ecol Evol, 7:489.
[30]ChenJ, MuellerV, 2018. Coastal climate change, soil salinity and human migration in Bangladesh. Nat Climate Change, 8(11):981-985.
[31]ChristenE, SaliemKA, 2013. Managing Salinity in Iraq’s Agriculture: Current State, Causes, and Impacts. International Center for Agricultural Research in the Dry Areas (ICARDA), Lebanon.
[32]CiaisP, ReichsteinM, ViovyN, et al., 2005. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature, 437(7058):529-533.
[33]CiancioN, MirallesDJ, StrikerGG, et al., 2021. Plant growth rate after, and not during, waterlogging better correlates to yield responses in wheat and barley. J Agron Crop Sci, 207(2):304-316.
[34]CochraneDW, ShahJK, HebelstrupKH, et al., 2017. Expression of phytoglobin affects nitric oxide metabolism and energy state of barley plants exposed to anoxia. Plant Sci, 265:124-130.
[35]CohenI, ZandalinasSI, HuckC, et al., 2021. Meta-analysis of drought and heat stress combination impact on crop yield and yield components. Physiol Plant, 171(1):66-76.
[36]CollinA, Daszkowska-GolecA, KurowskaM, et al., 2020. Barley ABI5 (Abscisic Acid INSENSITIVE 5) is involved in abscisic acid-dependent drought response. Front Plant Sci, 11:1138.
[37]ColmseeC, BeierS, HimmelbachA, et al., 2015. BARLEX-the barley draft genome explorer. Mol Plant, 8(6):964-966.
[38]CorwinDL, 2021. Climate change impacts on soil salinity in agricultural areas. Eur J Soil Sci, 72(2):842-862.
[39]DaliakopoulosIN, TsanisIK, KoutroulisA, et al., 2016. The threat of soil salinity: a European scale review. Sci Total Environ, 573:727-739.
[40]de CastroJ, HillRD, StasollaC, et al., 2022. Waterlogging stress physiology in barley. Agronomy, 12(4):780.
[41]de san CeledonioRP, AbeledoLG, MirallesDJ, 2014. Identifying the critical period for waterlogging on yield and its components in wheat and barley. Plant Soil, 378(1-2):265-277.
[42]DickinE, WrightD, 2008. The effects of winter waterlogging and summer drought on the growth and yield of winter wheat (Triticum aestivum L.). Eur J Agron, 28(3):234-244.
[43]DollNM, GillesLM, GérentesMF, et al., 2019. Single and multiple gene knockouts by CRISPR-Cas9 in maize. Plant Cell Rep, 38(4):487-501.
[44]ElliottJ, GlotterM, RuaneAC, et al., 2018. Characterizing agricultural impacts of recent large-scale US droughts and changing technology and management. Agric Syst, 159:275-281.
[45]FatimaZ, AhmedM, HussainM, et al., 2020. The fingerprints of climate warming on cereal crops phenology and adaptation options. Sci Rep, 10:18013.
[46]FengX, LiuWX, QiuCW, et al., 2020a. HvAKT2 and HvHAK1 confer drought tolerance in barley through enhanced leaf mesophyll H+ homoeostasis. Plant Biotechnol J, 18(8):1683-1696.
[47]FengX, LiuWX, CaoFB, et al., 2020b. Overexpression of HvAKT1 improves drought tolerance in barley by regulating root ion homeostasis and ROS and NO signaling. J Exp Bot, 71(20):6587-6600.
[48]FlessnerML, BurkeIC, DilleJA, et al., 2021. Potential wheat yield loss due to weeds in the United States and Canada. Weed Technol, 35(6):916-923.
[49]FAO (The Food and Agriculture Organization of the United Nations), 2009. Global Agriculture Towards 2050. High Level Expert Forum—How to Feed the World in 2050, Office of the Director, Agricultural Development Economics Division Economic and Social Development Department, Rome, Italy. https://www.fao.org/fileadmin/templates/wsfs/docs/Issues_papers/HLEF2050_Global_Agriculture.pdf
[50]FuLB, WuDZ, ZhangXC, et al., 2022. Vacuolar H+-pyrophosphatase HVP10 enhances salt tolerance via promoting Na+ translocation into root vacuoles. Plant Physiol, 188(2):1248-1263.
[51]FujiiM, YokoshoK, YamajiN, et al., 2012. Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun, 3:713.
[52]GalonL, BassoFJM, ForteCT, et al., 2022. Weed interference period and economic threshold level in barley. J Plant Prot Res, 62(1):33-48.
[53]GammansM, MérelP, Ortiz-BobeaA, 2017. Negative impacts of climate change on cereal yields: statistical evidence from France. Environ Res Lett, 12(5):054007.
[54]GaoYY, QuanSX, LyuB, et al., 2022. Barley transcription factor HvNLP2 mediates nitrate signaling and affects nitrogen use efficiency. J Exp Bot, 73(3):770-783.
[55]GasparisS, KałaM, PrzyborowskiM, et al., 2018. A simple and efficient CRISPR/Cas9 platform for induction of single and multiple, heritable mutations in barley (Hordeum vulgare L.). Plant Methods, 14:111.
[56]GengGP, WuJJ, WangQF, et al., 2016. Agricultural drought hazard analysis during 1980‒2008: a global perspective. Int J Climatol, 36(1):389-399.
[57]GhardeY, SinghPK, DubeyRP, 2018. Assessment of yield and economic losses in agriculture due to weeds in India. Crop Protection, 107:12-18.
[58]GierczikK, SzékelyA, AhresM, et al., 2019. Overexpression of two upstream phospholipid signaling genes improves cold stress response and hypoxia tolerance, but leads to developmental abnormalities in barley. Plant Mol Biol Rep, 37(4):314-326.
[59]Gomez-SanchezA, Gonzalez-MelendiP, SantamariaME, et al., 2019. Repression of drought-induced cysteine-protease genes alters barley leaf structure and responses to abiotic and biotic stresses. J Exp Bot, 70(7):2143-2155.
[60]GorjiT, SertelE, TanikA, 2017. Monitoring soil salinity via remote sensing technology under data scarce conditions: a case study from Turkey. Ecol Indic, 74:384-391.
[61]GRDCGrowNotes, 2016. Barley Weed Control, Barley Northern Region. https://grdc.com.au/__data/assets/pdf_file/0022/370534/GrowNote-Barley-North-6-Weed-Control.pdf
[62]GrohmannL, KeilwagenJ, DuensingN, et al., 2019. Detection and identification of genome editing in plants: challenges and opportunities. Front Plant Sci, 10:236.
[63]GürelF, ÖztürkZN, UçarlıC, et al., 2016. Barley genes as tools to confer abiotic stress tolerance in crops. Front Plant Sci, 7:1137.
[64]HanY, YinSY, HuangL, et al., 2018. A sodium transporter HvHKT1;1 confers salt tolerance in barley via regulating tissue and cell ion homeostasis. Plant Cell Physiol, 59(10):1976-1989.
[65]HanY, BroughtonS, LiuL, et al., 2021. Highly efficient and genotype-independent barley gene editing based on anther culture. Plant Commun, 2(2):100082.
[66]HazzouriKM, KhraiweshB, AmiriKMA, et al., 2018. Mapping of HKT1;5 gene in barley using GWAS approach and its implication in salt tolerance mechanism. Front Plant Sci, 9:156.
[67]HeG, LiuXS, CuiZL, 2021. Achieving global food security by focusing on nitrogen efficiency potentials and local production. Glob Food Sec, 29:100536.
[68]HeTH, AngessaT, HillCB, et al., 2022. Genetic solutions through breeding counteract climate change and secure barley production in Australia. Crop Des, 1(1):100001.
[69]HebelstrupKH, ShahJK, SimpsonC, et al., 2014. An assessment of the biotechnological use of hemoglobin modulation in cereals. Physiol Plant, 150(4):593-603.
[70]HefferP, Prud'hommeM, 2016. Global nitrogen fertiliser demand and supply: trend, current level and outlook. Proceedings of 2016 International Nitrogen Initiative Conference, Melbourne, Australia.
[71]HirayamaT, ShinozakiK, 2010. Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J, 61(6):1041-1052.
[72]HolmeIB, WendtT, Gil-HumanesJ, et al., 2017. Evaluation of the mature grain phytase candidate HvPAPhy_a gene in barley (Hordeum vulgare L.) using CRISPR/Cas9 and TALENs. Plant Mol Biol, 95(1-2):111-121.
[73]HoukE, FrasierM, SchuckE, 2006. The agricultural impacts of irrigation induced waterlogging and soil salinity in the Arkansas Basin. Agric Water Manag, 85(1-2):175-183.
[74]HoultonBZ, AlmarazM, AnejaV, et al., 2019. A world of cobenefits: solving the global nitrogen challenge. Earths Future, 7(8):865-872.
[75]HuangJP, YuHP, GuanXD, et al., 2016. Accelerated dryland expansion under climate change. Nat Climate Change, 6(2):166-171.
[76]HuangL, KuangLH, WuLY, et al., 2020. The HKT transporter HvHKT1;5 negatively regulates salt tolerance. Plant Physiol, 182(1):584-596.
[77]HudzenkoVM, DemydovOA, PolishchukTP, et al., 2021. Comprehensive evaluation of spring barley yield and tolerance to abiotic and biotic stresses. Ukr J Ecol, 11(8):48-55.
[78]HuffmanE, EilersRG, PadburyG, et al., 2000. Canadian agri-environmental indicators related to land quality: integrating census and biophysical data to estimate soil cover, wind erosion and soil salinity. Agric Ecosyst Environ, 81(2):113-123.
[79]HughesJ, HepworthC, DuttonC, et al., 2017. Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol, 174(2):776-787.
[80]HuntE, FemiaF, WerrellC, et al., 2021. Agricultural and food security impacts from the 2010 Russia flash drought. Weather Climate Extremes, 34:100383.
[81]The International Barley Genome Sequencing Consortium, 2012. A physical, genetic and functional sequence assembly of the barley genome. Nature, 491(7426):711-716.
[82]IsmagulA, MazonkaI, CallegariC, et al., 2014. Agrobacterium-mediated transformation of barley (Hordeum vulgare L.). In: Fleury D, Whitford R (Eds.), Crop Breeding: Methods and Protocols. Human Press, New York, p.203-211.
[83]JabranK, MahajanG, SardanaV, et al., 2015. Allelopathy for weed control in agricultural systems. Crop Protection, 72:57-65.
[84]JanackB, SosoiP, KrupinskaK, et al., 2016. Knockdown of WHIRLY1 affects drought stress-induced leaf senescence and histone modifications of the senescence-associated gene HvS40. Plants, 5(3):37.
[85]JaniakA, KwasniewskiM, SowaM, et al., 2018. No time to waste: transcriptome study reveals that drought tolerance in barley may be attributed to stressed-like expression patterns that exist before the occurrence of stress. Front Plant Sci, 8:2212.
[86]JayakodiM, PadmarasuS, HabererG, et al., 2020. The barley pan-genome reveals the hidden legacy of mutation breeding. Nature, 588(7837):284-289.
[87]JeknićZ, PillmanKA, DhillonT, et al., 2014. Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation. Plant Mol Biol, 84(1-2):67-82.
[88]KangGZ, LiGZ, MaHZ, et al., 2013. Proteomic analysis on the leaves of TaBTF3 gene virus-induced silenced wheat plants may reveal its regulatory mechanism. J Proteomics, 83:130-143.
[89]KarunarathneSD, HanY, ZhangXQ, et al., 2020. Genome-wide association study and identification of candidate genes for nitrogen use efficiency in barley (Hordeum vulgare L.). Front Plant Sci, 11:571912.
[90]KarunarathneSD, HanY, ZhangXQ, et al., 2022. CRISPR/Cas9 gene editing and natural variation analysis demonstrate the potential for HvARE1 in improvement of nitrogen use efficiency in barley. J Integr Plant Biol, 64(3):756-770.
[91]KebedeA, KangMS, BekeleE, 2019. Advances in mechanisms of drought tolerance in crops, with emphasis on barley. Adv Agron, 156:265-314.
[92]KershanskayaOI, YessenbaevaGL, NelidovaDS, et al., 2022. CRISPR/Cas genome editing perspectives for barley breeding. Physiol Plant, 174(3):e13686.
[93]KimYA, MoonH, ParkCJ, 2019. CRISPR/Cas9-targeted mutagenesis of Os8N3 in rice to confer resistance to Xanthomonas oryzae pv. oryzae. Rice, 12:67.
[94]KironoDGC, RoundV, HeadyC, et al., 2020. Drought projections for Australia: updated results and analysis of model simulations. Weather Climate Extremes, 30:100280.
[95]KlocY, Dmochowska-BogutaM, ZielezinskiA, et al., 2020. Silencing of HvGSK1.1―a GSK3/SHAGGY-like kinase―enhances barley (Hordeum vulgare L.) growth in normal and in salt stress conditions. Int J Mol Sci, 21(18):6616.
[96]KovalchukN, JiaW, EiniO, et al., 2013. Optimization of TaDREB3 gene expression in transgenic barley using cold-inducible promoters. Plant Biotechnol J, 11(6):659-670.
[97]KřenekP, ChubarE, VadovičP, et al., 2021. CRISPR/Cas9-induced loss-of-function mutation in the barley mitogen-activated protein kinase 6 gene causes abnormal embryo development leading to severely reduced grain germination and seedling shootless phenotype. Front Plant Sci, 12:670302.
[98]KubiakA, Wolna-MaruwkaA, NiewiadomskaA, et al., 2022. The problem of weed infestation of agricultural plantations vs. the assumptions of the European biodiversity strategy. Agronomy, 12(8):1808.
[99]KumarP, SahuNC, KumarS, et al., 2021. Impact of climate change on cereal production: evidence from lower-middle-income countries. Environ Sci Pollut Res, 28(37):51597-51611.
[100]KurnazL, 2014. Drought in Turkey. Istanbul Policy Center, Sabanci University, Istanbul. https://ipc.sabanciuniv.edu/Content/Images/CKeditorImages/20200323-16034498.pdf
[101]KuscuC, ParlakM, TufanT, et al., 2017. CRISPR-STOP: gene silencing through base-editing-induced nonsense mutations. Nat Methods, 14(7):710-712.
[102]LangholtzM, DavisonBH, JagerHI, et al., 2021. Increased nitrogen use efficiency in crop production can provide economic and environmental benefits. Sci Total Environ, 758:143602.
[103]LawrensonT, HarwoodWA, 2019. Creating targeted gene knockouts in barley using CRISPR/Cas9. In: Harwood WA (Ed.), Barley. Humana Press, New York, p.217-232.
[104]LawrensonT, ShorinolaO, StaceyN, et al., 2015. Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol, 16:258.
[105]LeongKYB, ChanYH, WMANWAbdullah, et al., 2018. The CRISPR/Cas9 system for crop improvement: progress and prospects. In: Çiftçi YÖ (Ed.), Next Generation Plant Breeding. IntechOpen, London, United Kingdom.
[106]LiC, ZhangR, MengXB, et al., 2020. Targeted, random mutagenesis of plant genes with dual cytosine and adenine base editors. Nat Biotechnol, 38(7):875-882.
[107]LiW, TengF, LiTD, et al., 2013. Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol, 31(8):684-686.
[108]LiangJJ, DengGB, LongH, et al., 2012. Virus-induced silencing of genes encoding LEA protein in Tibetan hulless barley (Hordeum vulgare ssp. vulgare) and their relationship to drought tolerance. Mol Breed, 30(1):441-451.
[109]LinQP, ZongY, XueCX, et al., 2020. Prime genome editing in rice and wheat. Nat Biotechnol, 38(5):582-585.
[110]LinQP, JinS, ZongY, et al., 2021. High-efficiency prime editing with optimized, paired pegRNAs in plants. Nat Biotechnol, 39(8):923-927.
[111]LiuK, HarrisonMT, IbrahimA, et al., 2020a. Genetic factors increasing barley grain yields under soil waterlogging. Food Energy Secur, 9(4):e238.
[112]LiuK, HarrisonMT, HuntJ, et al., 2020b. Identifying optimal sowing and flowering periods for barley in Australia: a modelling approach. Agric For Meteorol, 282-283:107871.
[113]LiuK, HarrisonMT, ShabalaS, et al., 2020c. The state of the art in modeling waterlogging impacts on plants: what do we know and what do we need to know. Earths Future, 8(12):e2020EF001801.
[114]LiuK, HarrisonMT, ArchontoulisSV, et al., 2021. Climate change shifts forward flowering and reduces crop waterlogging stress. Environ Res Lett, 16(9):094017.
[115]LiuK, HarrisonMT, YanHL, et al., 2023. Silver lining to a climate crisis in multiple prospects for alleviating crop waterlogging under future climates. Nat Commun, 14:765.
[116]LlewellynR, RonningD, OuzmanJ, et al., 2016. Impact of Weeds on Australian Grain Production: the Cost of Weeds to Australian Grain Growers and the Adoption of Weed Management and Tillage Practices. Technical Report No. EP161334, Grains Research and Development Corporation, Canberra, Australia. https://grdc.com.au/__data/assets/pdf_file/0027/75843/grdc_weeds_review_r8.pdf.pdf
[117]LowderLG, ZhouJP, ZhangYX, et al., 2018. Robust transcriptional activation in plants using multiplexed CRISPR-Act2.0 and mTALE-Act systems. Mol Plant, 11(2):245-256.
[118]LoweK, WuE, WangN, et al., 2016. Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell, 28(9):1998-2015.
[119]LuCQ, TianHQ, 2017. Global nitrogen and phosphorus fertilizer use for agriculture production in the past half century: shifted hot spots and nutrient imbalance. Earth Syst Sci Data, 9(1):181-192.
[120]MaXN, ZhangXY, LiuHM, et al., 2020. Highly efficient DNA-free plant genome editing using virally delivered CRISPR-Cas9. Nat Plants, 6(7):773-779.
[121]MahajanG, HickeyL, ChauhanBS, 2020. Response of barley genotypes to weed interference in Australia. Agronomy, 10(1):99.
[122]MaherMF, NastiRA, VollbrechtM, et al., 2020. Plant gene-editing through de novo induction of meristems. Nat Biotechnol, 38(1):84-89.
[123]ManikSMN, PengilleyG, DeanG, et al., 2019. Soil and crop management practices to minimize the impact of waterlogging on crop productivity. Front Plant Sci, 10:140.
[124]ManikSMN, QuamruzzamanM, LivermoreM, et al., 2022. Impacts of barley root cortical aerenchyma on growth, physiology, yield components, and grain quality under field waterlogging conditions. Field Crops Res, 279:108461.
[125]ManmathanH, ShanerD, SnellingJ, et al., 2013. Virus-induced gene silencing of Arabidopsis thaliana gene homologues in wheat identifies genes conferring improved drought tolerance. J Exp Bot, 64(5):1381-1392.
[126]MaoXD, LiuC, TongH, et al., 2019. Principles of digital PCR and its applications in current obstetrical and gynecological diseases. Am J Transl Res, 11(12):7209-7222.
[127]MarkonisY, KumarR, HanelM, et al., 2021. The rise of compound warm-season droughts in Europe. Sci Adv, 7(6):eabb9668.
[128]MascherM, GundlachH, HimmelbachA, et al., 2017. A chromosome conformation capture ordered sequence of the barley genome. Nature, 544(7651):427-433.
[129]MasudMB, McAllisterT, CordeiroMRC, et al., 2018. Modeling future water footprint of barley production in Alberta, Canada: implications for water use and yields to 2064. Sci Total Environ, 616-617:208-222.
[130]MayerováM, MadarasM, SoukupJ, 2018. Effect of chemical weed control on crop yields in different crop rotations in a long-term field trial. Crop Protection, 114:215-222.
[131]McCartyNS, GrahamAE, StudenáL, et al., 2020. Multiplexed CRISPR technologies for gene editing and transcriptional regulation. Nat Commun, 11:1281.
[132]MendiondoGM, GibbsDJ, Szurman-ZubrzyckaM, et al., 2016. Enhanced waterlogging tolerance in barley by manipulation of expression of the N-end rule pathway E3 ligase PROTEOLYSIS6. Plant Biotechnol J, 14(1):40-50.
[133]MianA, OomenRJFJ, IsayenkovS, et al., 2011. Over-expression of an Na+-and K+-permeable HKT transporter in barley improves salt tolerance. Plant J, 68(3):468-479.
[134]MittlerR, 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci, 11(1):15-19.
[135]MonatC, PadmarasuS, LuxT, et al., 2019. TRITEX: chromosome-scale sequence assembly of Triticeae genomes with open-source tools. Genome Biol, 20:284.
[136]Montilla-BascónG, RubialesD, HebelstrupKH, et al., 2017. Reduced nitric oxide levels during drought stress promote drought tolerance in barley and is associated with elevated polyamine biosynthesis. Sci Rep, 7:13311.
[137]MookkanM, Nelson-VasilchikK, HagueJ, et al., 2017. Selectable marker independent transformation of recalcitrant maize inbred B73 and sorghum P898012 mediated by morphogenic regulators BABY BOOM and WUSCHEL2. Plant Cell Rep, 36(9):1477-1491.
[138]MunnsR, TesterM, 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol, 59:651-681.
[139]MwandoE, HanY, AngessaTT, et al., 2020. Genome-wide association study of salinity tolerance during germination in barley (Hordeum vulgare L.). Front Plant Sci, 11:118.
[140]MwendwaJM, BrownWB, WestonPA, et al., 2022. Evaluation of barley cultivars for competitive traits in Southern New South Wales. Plants, 11(3):362.
[141]NaeemM, FarooqS, HussainM, 2022. The impact of different weed management systems on weed flora and dry biomass production of barley grown under various barley-based cropping systems. Plants, 11(6):718.
[142]NagahatennaDSK, ParentB, EdwardsEJ, et al., 2020. Barley plants overexpressing Ferrochelatases (HvFC1 and HvFC2) show improved photosynthetic rates and have reduced photo-oxidative damage under drought stress than non-transgenic controls. Agronomy, 10(9):1351.
[143]NajeraVA, TwymanRM, ChristouP, et al., 2019. Applications of multiplex genome editing in higher plants. Curr Opin Biotechnol, 59:93-102.
[144]Nefissi OuertaniR, ArasappanD, AbidG, et al., 2021. Transcriptomic analysis of salt-stress-responsive genes in barley roots and leaves. Int J Mol Sci, 22(15):8155.
[145]NejatN, 2022. Gene Editing of Elite Malting Barley Cultivar RGT Planet Using Agrobacterium-Mediated Delivery of CRISPR/Cas9. PhD Thesis, Murdoch University, Perth, Australia.
[146]NejatN, HanY, ZhangXQ, et al., 2022. Swiftly evolving CRISPR genome editing: a revolution in genetic engineering for developing stress-resilient crops. Curr Chin Sci, 2(5):382-399.
[147]NonakaS, AraiC, TakayamaM, et al., 2017. Efficient increase of γ-aminobutyric acid (GABA) content in tomato fruits by targeted mutagenesis. Sci Rep, 7:7057.
[148]OerkeEC, 2006. Crop losses to pests. J Agric Sci, 144(1):31-43.
[149]Office of the Auditor General-Western Australia, 2018. Management of Salinity (Report 8‒May 2018). Office of the Auditor General Western Australia, Perth, Australia. https://audit.wa.gov.au/wp-content/uploads/2018/05/report2018_08-Salinity-2.pdf
[150]OtkinJA, SvobodaM, HuntED, et al., 2018. Flash droughts: a review and assessment of the challenges imposed by rapid-onset droughts in the United States. Bull Amer Meteor Soc, 99(5):911-919.
[151]OtkinJA, ZhongYF, HuntED, et al., 2021. Development of a flash drought intensity index. Atmosphere, 12(6):741.
[152]PanR, DingMQ, FengZB, et al., 2022. HvGST4 enhances tolerance to multiple abiotic stresses in barley: evidence from integrated meta-analysis to functional verification. Plant Physiol Biochem, 188:47-59.
[153]ParkerT, GallantA, HobbinsM, et al., 2021. Flash drought in Australia and its relationship to evaporative demand. Environ Res Lett, 16(6):064033.
[154]PaynterBH, HillsAL, 2009. Barley and rigid ryegrass (Lolium rigidum) competition is influenced by crop cultivar and density. Weed Technol, 23(1):40-48.
[155]PellegrinoE, BediniS, NutiM, et al., 2018. Impact of genetically engineered maize on agronomic, environmental and toxicological traits: a meta-analysis of 21 years of field data. Sci Rep, 8:3113.
[156]PetersonBA, HaakDC, NishimuraMT, et al., 2016. Genome-wide assessment of efficiency and specificity in CRISPR/Cas9 mediated multiple site targeting in Arabidopsis. PLoS ONE, 11(9):e0162169.
[157]QadirM, QuillérouE, NangiaV, et al., 2014. Economics of salt‐induced land degradation and restoration. Nat Resour Forum, 38(4):282-295.
[158]RenBZ, MaZT, ZhaoB, et al., 2022. Nitrapyrin mitigates nitrous oxide emissions, and improves maize yield and nitrogen efficiency under waterlogged field. Plants, 11(15):1983.
[159]RenC, LiHY, LiuYF, et al., 2022. Highly efficient activation of endogenous gene in grape using CRISPR/dCas9-based transcriptional activators. Hortic Res, 9:uhab037.
[160]RengasamyP, 2006. World salinization with emphasis on Australia. J Exp Bot, 57(5):1017-1023.
[161]RengasamyP, ChittleboroughD, HelyarK, 2003. Root-zone constraints and plant-based solutions for dryland salinity. Plant Soil, 257(2):249-260.
[162]RukhovichDI, SimakovaMS, KulyanitsaAL, et al., 2014. Impact of shelterbelts on the fragmentation of erosional networks and local soil waterlogging. Eurasian Soil Sci, 47(11):1086-1099.
[163]SafonovG, SafonovaY, 2013. Economic Analysis of the Impact of Climate Change on Agriculture in Russia: National and Regional Aspects. Oxfam Research Reports, Oxfam International House, Oxford.
[164]SamsonJ, BerteauxD, McGillBJ, et al., 2011. Geographic disparities and moral hazards in the predicted impacts of climate change on human populations. Glob Ecol Biogeogr, 20(4):532-544.
[165]SchmittJ, OffermannF, SöderM, et al., 2022. Extreme weather events cause significant crop yield losses at the farm level in German agriculture. Food Policy, 112:102359.
[166]SchreiberM, MascherM, WrightJ, et al., 2020. A genome assembly of the barley ‘transformation reference’ cultivar golden promise. G3-Genes Genom Genet, 10(6):1823-1827.
[167]SetterTL, WatersI, 2003. Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil, 253(1):1-34.
[168]ShimataniZ, KashojiyaS, TakayamaM, et al., 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol, 35(5):441-443.
[169]SivamaniE, BahieldinA, WraithJM, et al., 2000. Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci, 155(1):1-9.
[170]SmargonAA, CoxDBT, PyzochaNK, et al., 2017. Cas13b is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol Cell, 65(4):618-630.e7.
[171]SorokinA, BryzzhevA, StrokovA, et al., 2016. The economics of land degradation in Russia. In: Nkonya E, Mirzabaev A, von Braun J (Eds.), Economics of Land Degradation and Improvement—A Global Assessment for Sustainable Development. Springer, Cham, p.541-576.
[172]StahlK, KohnI, BlauhutV, et al., 2016. Impacts of European drought events: insights from an international database of text-based reports. Nat Hazards Earth Syst Sci, 16(3):801-819.
[173]Statista, 2022a. Major Barley Producers Worldwide in 2021/2022, by Country. https://www.statista.com/statistics/272760/barley-harvest-forecast
[174]Statista, 2022b. Worldwide Production of Grain in 2021/22, by Type. https://www.statista.com/statistics/263977/world-grain-production-by-type
[175]SunHY, ChenZH, ChenF, et al., 2015. DNA microarray revealed and RNAi plants confirmed key genes conferring low Cd accumulation in barley grains. BMC Plant Biol, 15:259.
[176]TalamèV, OzturkNZ, BohnertHJ, et al., 2007. Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J Exp Bot, 58(2):229-240.
[177]TaleisnikE, LavadoRS, 2021. Saline and Alkaline Soils in Latin America. Springer, Cham, Germany.
[178]Tello-RuizMK, JaiswalP, WareD, 2022. Gramene: a resource for comparative analysis of plants genomes and pathways. In: Edwards D (Ed.), Plant Bioinformatics. Humana, New York, p.101-131.
[179]TianLX, ZhangYC, ChenPL, et al., 2021. How does the waterlogging regime affect crop yield? A global meta-analysis. Front Plant Sci, 12:634898.
[180]TianSW, JiangLJ, CuiXX, et al., 2018. Engineering herbicide-resistant watermelon variety through CRISPR/Cas9-mediated base-editing. Plant Cell Rep, 37(9):1353-1356.
[181]TommasiniL, SvenssonJT, RodriguezEM, et al., 2008. Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.). Funct Integr Genomics, 8(4):387-405.
[182]MapTrade, 2022. Trade Statistics for International Business Development. https://www.trademap.org/Index.aspx
[183]TricaseC, AmicarelliV, LamonacaE, et al., 2018. Economic analysis of the barley market and related uses. In: Tadele Z (Ed.), Grasses as Food and Feed. IntechOpen, London, United Kingdom.
[184]TwiningS, 2014. Impact of 2014 Winter Floods on Agriculture in England. ADAS Ltd., UK. https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/401235/RFI7086_Flood_Impacts_Report__2_.pdf
[185]UllahA, BanoA, KhanN, 2021. Climate change and salinity effects on crops and chemical communication between plants and plant growth-promoting microorganisms under stress. Front Sustain Food Syst, 5:618092.
[186]UmezawaT, FujitaM, FujitaY, et al., 2006. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol, 17(2):113-122.
[187]USDA-FAS-IPAD (United States Department of Agriculture, Foreign Agricultural Service, International Production Assessment Division), 2022. Crop Production Maps. United States Government. https://ipad.fas.usda.gov/ogamaps/cropproductionmaps.aspx
[188]van DijkM, MorleyT, RauML, et al., 2021. A meta-analysis of projected global food demand and population at risk of hunger for the period 2010‒2050. Nat Food, 2(7):494-501.
[189]van VeelenB, 2021. Cash cows? Assembling low-carbon agriculture through green finance. Geoforum, 118:130-139.
[190]Velasco‐ArroyoB, Diaz‐MendozaM, Gomez‐SanchezA, et al., 2018. Silencing barley cystatins HvCPI‐2 and HvCPI‐4 specifically modifies leaf responses to drought stress. Plant Cell Environ, 41(8):1776-1790.
[191]VisioniA, Al-AbdallatA, ElenienJA, et al., 2019. Genomics and molecular breeding for improving tolerance to abiotic stress in barley (Hordeum vulgare L.). In: Rajpal VR, Sehgal D, Kumar A, et al. (Eds.), Genomics Assisted Breeding of Crops for Abiotic Stress Tolerance, Vol. II. Springer, Cham, p.49-68.
[192]VlčkoT, OhnoutkováL, 2020. Allelic variants of CRISPR/Cas9 induced mutation in an inositol trisphosphate 5/6 kinase gene manifest different phenotypes in barley. Plants, 9(2):195.
[193]WadaN, UetaR, OsakabeY, et al., 2020. Precision genome editing in plants: state-of-the-art in CRISPR/Cas9-based genome engineering. BMC Plant Biol, 20:234.
[194]WanY, LemauxPG, 1994. Generation of large numbers of independently transformed fertile barley plants. Plant Physiol, 104(1):37-48.
[195]WangJ, VangaSK, SaxenaR, et al., 2018. Effect of climate change on the yield of cereal crops: a review. Climate, 6(2):41.
[196]WangK, ShiL, LiangXN, et al., 2022. The gene TaWOX5 overcomes genotype dependency in wheat genetic transformation. Nat Plants, 8(2):110-117.
[197]WangWQ, ZhangGQ, YangSL, et al., 2021. Overexpression of isochorismate synthase enhances drought tolerance in barley. J Plant Physiol, 260:153404.
[198]WaniSH, KumarV, KhareT, et al., 2020. Engineering salinity tolerance in plants: progress and prospects. Planta, 251(4):76.
[199]WardlawIF, WrigleyCW, 1994. Heat tolerance in temperate cereals: an overview. Aust J Plant Physiol, 21(6):695-703.
[200]WolfeD, DudekS, RitchieMD, et al., 2013. Visualizing genomic information across chromosomes with PhenoGram. BioData Min, 6:18.
[201]XieW, XiongW, PanJ, et al., 2018. Decreases in global beer supply due to extreme drought and heat. Nat Plants, 4(11):964-973.
[202]XingHL, DongL, WangZP, et al., 2014. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol, 14:327.
[203]XiongXY, LiZX, LiangJP, et al., 2022. A cytosine base editor toolkit with varying activity windows and target scopes for versatile gene manipulation in plants. Nucleic Acids Res, 50(6):3565-3580.
[204]XuRF, LiJ, LiuXS, et al., 2020. Development of plant prime-editing systems for precise genome editing. Plant Commun, 1(3):100043.
[205]YanHL, HarrisonMT, LiuK, et al., 2022. Crop traits enabling yield gains under more frequent extreme climatic events. Sci Total Environ, 808:152170.
[206]YanM, PanGX, LavalleeJM, et al., 2020. Rethinking sources of nitrogen to cereal crops. Glob Chang Biol, 26(1):191-199.
[207]YangSH, KimE, ParkH, et al., 2022. Selection of the high efficient sgRNA for CRISPR-Cas9 to edit herbicide related genes, PDS, ALS, and EPSPS in tomato. Appl Biol Chem, 65:13.
[208]YavasI, UnayA, AydinM, 2012. The waterlogging tolerance of wheat varieties in western of Turkey. Sci World J, 2012:529128.
[209]ZahraN, HafeezMB, ShaukatK, et al., 2021. Hypoxia and anoxia stress: plant responses and tolerance mechanisms. J Agron Crop Sci, 207(2):249-284.
[210]ZaidiSSEA, MahfouzMM, MansoorS, 2017. CRISPR-Cpf1: a new tool for plant genome editing. Trends Plant Sci, 22(7):550-553.
[211]ZamanM, ShahidSA, HengL, 2018. Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques. Springer, Cham, Germany.
[212]ZangYM, GongQ, XuYH, et al., 2022. Production of conjoined transgenic and edited barley and wheat plants for Nud genes using the CRISPR/SpCas9 system. Front Genet, 13:873850.
[213]ZengZH, HanN, LiuCC, et al., 2020. Functional dissection of HGGT and HPT in barley vitamin E biosynthesis via CRISPR/Cas9-enabled genome editing. Ann Bot, 126(5):929-942.
[214]ZhangJH, ZhangHT, LiSY, et al., 2021. Increasing yield potential through manipulating of an ARE1 ortholog related to nitrogen use efficiency in wheat by CRISPR/Cas9. J Integr Plant Biol, 63(9):1649-1663.
[215]ZhongYX, BlennowA, Kofoed-EnevoldsenO, et al., 2019. Protein Targeting to Starch 1 is essential for starchy endosperm development in barley. J Exp Bot, 70(2):485-496.
[216]ZhouGF, DelhaizeE, ZhouMX, et al., 2013. The barley MATE gene, HvAACT1, increases citrate efflux and Al3+ tolerance when expressed in wheat and barley. Ann Bot, 112(3):603-612.
[217]ZhouGF, BroughtonS, ZhangXQ, et al., 2016. Genome-wide association mapping of acid soil resistance in barley (Hordeum vulgare L.). Front Plant Sci, 7:406.
[218]ZhuHC, LiC, GaoCX, 2020. Applications of CRISPR-Cas in agriculture and plant biotechnology. Nat Rev Mol Cell Biol, 21(11):661-677.
[219]ZhuHD, 2005. Single-strand conformational polymorphism analysis: basic principles and routine practice. In: Fennell JP, Baker AH (Eds.), Hypertension. Humana Press, Humana Totowa, p.149-158.
Open peer comments: Debate/Discuss/Question/Opinion
<1>