Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Comprehensive analysis of potato (Solanum tuberosum) PYL genes highlights their role in stress responses

Shareef Gul A # , Hameed Gul A # , Muhammad Shahzad B , Ikram Ullah C , Ali Shahzad https://orcid.org/0009-0007-5520-3760 A D E * and Shahid Ullah Khan https://orcid.org/0009-0005-0741-0779 A F *
+ Author Affiliations
- Author Affiliations

A College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China.

B Department of Agronomy, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China.

C College of Resources and Environment, Southwest University, Chongqing 400715, China.

D Sanya Nanfan Research Institute of Hainan University, Sanya, 572025, China.

E College of Tropical Crops, Hainan University, Haikou, 570288, China.

F Women Medical and Dental College, Khyber Medical University, Peshawar, KPK 22020, Pakistan.

# These authors contributed equally to this paper

Handling Editor: Inzamam Haq

Functional Plant Biology 51, FP24094 https://doi.org/10.1071/FP24094
Submitted: 26 March 2024  Accepted: 29 June 2024  Published: 18 July 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Abscisic acid (ABA) regulates plant development, seed germination, and stress responses. The PYR1-like (PYL) proteins are essential for ABA signalling. However, the evolution and expression of PYL genes in potato (Solanum tuberosum) remain poorly understood. Here, we analysed and identified 17 PYL genes in the potato genome, which were categorised into three groups based on phylogenetic analysis. These genes are distributed across nine chromosomes with predicted proteins subcellar localisation primarily in the cytoplasm. These StPYLs revealed conserved exon structures and domains among the groups. Promoter region analysis indicated hormone and stress-related elements in all StPYLs. Protein–protein interactions and microRNA networks predicted that the interactions of StPYLs are crucial components of ABA signalling, underlining their pivotal role in stress management and growth regulation in potato. Expression profiling across different tissues and under various stresses revealed their varied expression pattern. Further, we validated the expression pattern of selected StPYLs through reverse transcription quantitative PCR under drought, salt, and Phytophthora infestans stresses. This revealed consistent upregulation of StPYL6 in these stresses, while StPYL11 exhibited significant downregulation over time. Other genes showed downregulation under drought and salt stresses while upregulation under P. infestans. Overall, our results suggested the potential role of PYL genes in abiotic and biotic stresses.

Keywords: ABA signalling, biotic and abiotic stresses, conserved domains, different tissues, expression profile, genome-wide analysis, PYL gene family, Solanum tuberosum L.

References

ain-Ali Q-U, Mushtaq N, Amir R, Gul A, Tahir M, Munir F (2021) Genome-wide promoter analysis, homology modeling and protein interaction network of Dehydration Responsive Element Binding (DREB) gene family in Solanum tuberosum. PLoS ONE 16(12), e0261215.
| Crossref | Google Scholar | PubMed |

Ali F, Qanmber G, Li F, Wang Z (2022) Updated role of ABA in seed maturation, dormancy, and germination. Journal of Advanced Research 35, 199-214.
| Crossref | Google Scholar | PubMed |

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25(17), 3389-3402.
| Crossref | Google Scholar | PubMed |

An Y, Mi X, Xia X, Qiao D, Yu S, Zheng H, Jing T, Zhang F (2023) Genome-wide identification of the PYL gene family of tea plants (Camellia sinensis) revealed its expression profiles under different stress and tissues. BMC Genomics 24(1), 362.
| Crossref | Google Scholar | PubMed |

Bai G, Xie H, Yao H, Li F, Chen X, Zhang Y, Xiao B, Yang J, Li Y, Yang D-H (2019) Genome-wide identification and characterization of ABA receptor PYL/RCAR gene family reveals evolution and roles in drought stress in Nicotiana tabacum. BMC Genomics 20(1), 575.
| Crossref | Google Scholar |

Billah SA, Khan NZ, Ali W, Aasim M, Usman M, Alezzawi MA, Ullah H (2022) Genome-wide in silico identification and characterization of the stress associated protein (SAP) gene family encoding A20/AN1 zinc-finger proteins in potato (Solanum tuberosum L.). PLoS ONE 17(8), e0273416.
| Crossref | Google Scholar | PubMed |

Bonthala VS, Stich B (2024) StCoExpNet: a global co-expression network analysis facilitates identifying genes underlying agronomic traits in potatoes. Plant Cell Reports 43(5), 117.
| Crossref | Google Scholar |

Chen K, Li G-J, Bressan RA, Song C-P, Zhu J-K, Zhao Y (2020a) Abscisic acid dynamics, signaling, and functions in plants. Journal of Integrative Plant Biology 62(1), 25-54.
| Crossref | Google Scholar | PubMed |

Chen J, Pan A, He S, Su P, Yuan X, Zhu S, Liu Z (2020b) Different microRNA families involved in regulating high temperature stress response during cotton (Gossypium hirsutum L.) anther development. International Journal of Molecular Sciences 21(4), 1280.
| Crossref | Google Scholar | PubMed |

Chou K-C, Shen H-B (2010) Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5(6), e11335.
| Crossref | Google Scholar | PubMed |

Chourasia KN, Lal MK, Tiwari RK, Dev D, Kardile HB, Patil VU, Kumar A, Vanishree G, Kumar D, Bhardwaj V, Meena JK, Mangal V, Shelake RM, Kim J-Y, Pramanik D (2021) Salinity stress in potato: understanding physiological, biochemical and molecular responses. Life 11(6), 545.
| Crossref | Google Scholar | PubMed |

Clark BJ (2020) The START-domain proteins in intracellular lipid transport and beyond. Molecular and Cellular Endocrinology 504, 110704.
| Crossref | Google Scholar | PubMed |

Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18), 3674-3676.
| Crossref | Google Scholar | PubMed |

Cui Y-X, Xu Z-C, Chen X-L, Nie L-P, Wu L-W, Wang Y, Song J-Y, Yao H (2020) Genome-wide identification of abscisic acid (ABA) receptor pyrabactin resistance 1-like protein (PYL) family members and expression analysis of PYL genes in response to different concentrations of ABA stress in Glycyrrhiza uralensis. Chinese Journal of Natural Medicines 18(8), 606-611.
| Crossref | Google Scholar |

del Mar Martínez-Prada M, Curtin SJ, Gutiérrez-González JJ (2021) Potato improvement through genetic engineering. GM Crops & Food 12(1), 479-496.
| Crossref | Google Scholar | PubMed |

Deng K, Yin H, Xiong F, Feng L, Dong P, Ren M (2021) Genome-wide miRNA expression profiling in potato (Solanum tuberosum L.) reveals TOR-dependent post-transcriptional gene regulatory networks in diverse metabolic pathway. PeerJ 9, e10704.
| Crossref | Google Scholar | PubMed |

Denham T, Barton H, Castillo C, Crowther A, Dotte-Sarout E, Florin SA, Pritchard J, Barron A, Zhang Y, Fuller DQ (2020) The domestication syndrome in vegetatively propagated field crops. Annals of Botany 125(4), 581-597.
| Crossref | Google Scholar | PubMed |

Di F, Jian H, Wang T, Chen X, Ding Y, Du H, Lu K, Li J, Liu L (2018) Genome-wide analysis of the PYL gene family and identification of PYL genes that respond to abiotic stress in Brassica napus. Genes 9(3), 156.
| Crossref | Google Scholar | PubMed |

Dittrich M, Mueller HM, Bauer H, Peirats-Llobet M, Rodriguez PL, Geilfus C-M, Carpentier SC, Al Rasheid KAS, Kollist H, Merilo E, Herrmann J, Müller T, Ache P, Hetherington AM, Hedrich R (2019) The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nature Plants 5(9), 1002-1011.
| Crossref | Google Scholar | PubMed |

Fernando VD, Schroeder DF (2016) Role of ABA in Arabidopsis salt, drought, and desiccation tolerance. In ‘Abiotic and biotic stress in plants-recent advances and future perspectives’. (Eds AK Shanker, C Shanker). (IntechOpen). doi:10.5772/61957

García-Andrade J, González B, Gonzalez-Guzman M, Rodriguez PL, Vera P (2020) The role of ABA in plant immunity is mediated through the PYR1 receptor. International Journal of Molecular Sciences 21, 5852.
| Crossref | Google Scholar | PubMed |

Ghorbel M, Brini F, Sharma A, Landi M (2021) Role of jasmonic acid in plants: the molecular point of view. Plant Cell Reports 40, 1471-1494.
| Crossref | Google Scholar | PubMed |

Gietler M, Fidler J, Labudda M, Nykiel M (2020) Abscisic acid—enemy or savior in the response of cereals to abiotic and biotic stresses? International Journal of Molecular Sciences 21, 4607.
| Crossref | Google Scholar | PubMed |

Guo D, Zhou Y, Li H-L, Zhu J-H, Wang Y, Chen X-T, Peng S-Q (2017) Identification and characterization of the abscisic acid (ABA) receptor gene family and its expression in response to hormones in the rubber tree. Scientific Reports 7(1), 45157.
| Crossref | Google Scholar |

Hao Q, Yin P, Li W, Wang L, Yan C, Lin Z, Wu JZ, Wang J, Yan SF, Yan N (2011) The molecular basis of ABA-independent inhibition of PP2Cs by a subclass of PYL proteins. Molecular Cell 42(5), 662-672.
| Crossref | Google Scholar | PubMed |

He Z, Zhong J, Sun X, Wang B, Terzaghi W, Dai M (2018) The maize ABA receptors ZmPYL8, 9, and 12 facilitate plant drought resistance. Frontiers in Plant Science 9, 422.
| Crossref | Google Scholar | PubMed |

Hou H, Lv L, Huo H, Dai H, Zhang Y (2020) Genome-wide identification of the ABA receptors genes and their response to abiotic stress in apple. Plants 9(8), 1028.
| Crossref | Google Scholar | PubMed |

Huang S, Wang C, Ding Z, Zhao Y, Dai J, Li J, Huang H, Wang T, Zhu M, Feng M, Ji Y, Zhang Z, Tao X (2024) A plant NLR receptor employs ABA central regulator PP2C-SnRK2 to activate antiviral immunity. Nature Communications 15(1), 3205.
| Crossref | Google Scholar |

Jennings SA, Koehler A-K, Nicklin KJ, Deva C, Sait SM, Challinor AJ (2020) Global potato yields increase under climate change with adaptation and CO2 fertilisation. Frontiers in Sustainable Food Systems 4, 519324.
| Crossref | Google Scholar |

Jing Z, Liu N, Zhang Z, Hou X (2024) Research progress on plant responses to stress combinations in the context of climate change. Plants 13(4), 469.
| Crossref | Google Scholar | PubMed |

Kim H, Lee K, Hwang H, Bhatnagar N, Kim D-Y, Yoon IS, Byun M-O, Kim ST, Jung K-H, Kim B-G (2014) Overexpression of PYL5 in rice enhances drought tolerance, inhibits growth, and modulates gene expression. Journal of Experimental Botany 65(2), 453-464.
| Crossref | Google Scholar | PubMed |

Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6), 1547-1549.
| Crossref | Google Scholar | PubMed |

Lamers J, van Der Meer T, Testerink C (2020) How plants sense and respond to stressful environments. Plant Physiology 182(4), 1624-1635.
| Crossref | Google Scholar | PubMed |

Lee SH, Oh SH, Hwang IG, Kim HY, Woo KS, Woo SH, Kim HS, Lee J, Jeong HS (2016) Antioxidant contents and antioxidant activities of white and colored potatoes (Solanum tuberosum L.). Preventive Nutrition and Food Science 21(2), 110-116.
| Crossref | Google Scholar | PubMed |

Lei P, Wei X, Gao R, Huo F, Nie X, Tong W, Song W (2021) Genome-wide identification of PYL gene family in wheat: evolution, expression and 3D structure analysis. Genomics 113(2), 854-866.
| Crossref | Google Scholar | PubMed |

Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49(W1), W293-W296.
| Crossref | Google Scholar | PubMed |

Letunic I, Khedkar S, Bork P (2021) SMART: recent updates, new developments and status in 2020. Nucleic Acids Research 49(D1), D458-D460.
| Crossref | Google Scholar | PubMed |

Li Y, Wang Y, Tan S, Li Z, Yuan Z, Glanc M, Domjan D, Wang K, Xuan W, Guo Y, Gong Z, Friml J, Zhang J (2020) Root growth adaptation is mediated by PYLs ABA receptor-PP2A protein phosphatase complex. Advanced Science 7(3), 1901455.
| Crossref | Google Scholar | PubMed |

Liu Z, Li Y, Zhu J, Ma W, Li Z, Bi Z, Sun C, Bai J, Zhang J, Liu Y (2021) Genome-wide identification and analysis of the NF-Y gene family in potato (Solanum tuberosum L.). Frontiers in Genetics 12, 739989.
| Crossref | Google Scholar | PubMed |

Liu S, Lu C, Jiang G, Zhou R, Chang Y, Wang S, Wang D, Niu J, Wang Z (2022) Comprehensive functional analysis of the PYL-PP2C-SnRK2s family in Bletilla striata reveals that BsPP2C22 and BsPP2C38 interact with BsPYLs and BsSnRK2s in response to multiple abiotic stresses. Frontiers in Plant Science 13, 963069.
| Crossref | Google Scholar | PubMed |

Liu Z, Zhang M, Wang L, Sun W, Li M, Feng C, Yang X (2023) Genome-wide identification and expression analysis of PYL family genes and functional characterization of GhPYL8D2 under drought stress in Gossypium hirsutum. Plant Physiology and Biochemistry 203, 108072.
| Crossref | Google Scholar | PubMed |

Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324(5930), 1064-1068.
| Crossref | Google Scholar | PubMed |

Maqsood H, Munir F, Amir R, Gul A (2022) Genome-wide identification, comprehensive characterization of transcription factors, cis-regulatory elements, protein homology, and protein interaction network of DREB gene family in Solanum lycopersicum. Frontiers in Plant Science 13, 1031679.
| Crossref | Google Scholar | PubMed |

Marand AP, Eveland AL, Kaufmann K, Springer NM (2023) cis-Regulatory elements in plant development, adaptation, and evolution. Annual Review of Plant Biology 74, 111-137.
| Crossref | Google Scholar | PubMed |

Mega R, Abe F, Kim J-S, Tsuboi Y, Tanaka K, Kobayashi H, Sakata Y, Hanada K, Tsujimoto H, Kikuchi J, Cutler SR, Okamoto M (2019) Tuning water-use efficiency and drought tolerance in wheat using abscisic acid receptors. Nature Plants 5(2), 153-159.
| Crossref | Google Scholar | PubMed |

Mehari TG, Xu Y, Umer MJ, Shiraku ML, Hou Y, Wang Y, Yu S, Zhang X, Wang K, Cai X, Zhou Z, Liu F (2021) Multi-omics-based identification and functional characterization of Gh_A06G1257 proves its potential role in drought stress tolerance in Gossypium hirsutum. Frontiers in Plant Science 12, 746771.
| Crossref | Google Scholar | PubMed |

Mohammadi F, Naghavi MR, Peighambari SA, Khosravi Dehaghi N, Khaldari I, Bravi E, Marconi O, Perretti G (2021) Abscisic acid crosstalk with auxin and ethylene in biosynthesis and degradation of inulin-type fructans in chicory. Plant Biology 23(4), 636-642.
| Crossref | Google Scholar | PubMed |

Muhammad Aslam M, Waseem M, Jakada BH, Okal EJ, Lei Z, Saqib HSA, Yuan W, Xu W, Zhang Q (2022) Mechanisms of abscisic acid-mediated drought stress responses in plants. International Journal of Molecular Sciences 23(3), 1084.
| Crossref | Google Scholar |

Narsing Rao MP, Lohmaneeratana K, Bunyoo C, Thamchaipenet A (2022) Actinobacteria–plant interactions in alleviating abiotic stress. Plants 11(21), 2976.
| Crossref | Google Scholar | PubMed |

Nasir MW, Toth Z (2022) Effect of drought stress on potato production: a review. Agronomy 12(3), 635.
| Crossref | Google Scholar |

Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-FF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324(5930), 1068-1071.
| Crossref | Google Scholar | PubMed |

Pieczynski M, Wyrzykowska A, Milanowska K, Boguszewska-Mankowska D, Zagdanska B, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2018) Genomewide identification of genes involved in the potato response to drought indicates functional evolutionary conservation with Arabidopsis plants. Plant Biotechnology Journal 16(2), 603-614.
| Crossref | Google Scholar |

Rani V, Singh VK, Joshi DC, Singh R, Yadav D (2024) Molecular docking insights into nuclear factor Y (NF-Y) transcription factor and pyrabactin resistance 1 (PYL) receptor proteins reveal abiotic stress regulation in finger millet. Crop Design 3(1), 100051.
| Crossref | Google Scholar |

Satheesh V, Chidambaranathan P, Jagannadham PT, Kohli D, Jain PK, Bhat SR, Srinivasan R (2014) A polyketide cyclase/dehydrase and lipid transport superfamily gene of Arabidopsis and its orthologue of chickpea exhibit rapid response to wounding. Indian Journal of Genetics and Plant Breeding 74, 463-470.
| Crossref | Google Scholar |

Shahzad A, Qian M, Sun B, Mahmood U, Li S, Fan Y, Chang W, Dai L, Zhu H, Li J, Qu C, Lu K (2021) Genome-wide association study identifies novel loci and candidate genes for drought stress tolerance in rapeseed. Oil Crop Science 6(1), 12-22.
| Crossref | Google Scholar |

Shahzad A, Gul H, Ahsan M, Wang D, Fahad S (2023a) Comparative genetic evaluation of maize inbred lines at seedling and maturity stages under drought stress. Journal of Plant Growth Regulation 42(2), 989-1005.
| Crossref | Google Scholar |

Shahzad A, Shahzad M, Imran M, Gul H, Gul S (2023b) Genome wide identification and expression profiling of PYL genes in barley. Plant Gene 36, 100434.
| Crossref | Google Scholar |

Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Current Opinion in Chemical Biology 7(2), 285-295.
| Crossref | Google Scholar | PubMed |

Shin IS, Chun J, Kim S, Cho K, Won K, Jung H, Kim K (2022) Transcriptomic profile in pear leave with resistance against Venturia nashicola infection. In ‘Proceedings of the Plant Resources Society of Korea Conference’. pp. 36–36. (The Plant Resources Society of Korea)

Siano AB, Roskruge N, Kerckhoffs H, Sofkova-Bobcheva S (2024) Effects of abiotic stress associated with climate change on potato yield and tuber quality under a multi-environment trial in New Zealand. Potato Research 6, 1-22.
| Google Scholar |

Singh B, Salaria N, Thakur K, Kukreja S, Gautam S, Goutam U (2019) Functional genomic approaches to improve crop plant heat stress tolerance. F1000Research 8, 1721.
| Google Scholar |

Sinha M, Singh RP, Kushwaha GS, Iqbal N, Singh A, Kaushik S, Kaur P, Sharma S, Singh TP (2014) Current overview of allergens of plant pathogenesis related protein families. The Scientific World Journal 2014, 543195.
| Crossref | Google Scholar | PubMed |

Soma F, Mogami J, Yoshida T, Abekura M, Takahashi F, Kidokoro S, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2017) ABA-unresponsive SnRK2 protein kinases regulate mRNA decay under osmotic stress in plants. Nature Plants 3(1), 16204.
| Crossref | Google Scholar |

Tiwari JK, Buckseth T, Zinta R, Bhatia N, Dalamu D, Naik S, Poonia AK, Kardile HB, Challam C, Singh RK, Luthra SK, Kumar V, Kumar M (2022) Germplasm, breeding, and genomics in potato improvement of biotic and abiotic stresses tolerance. Frontiers in Plant Science 13, 805671.
| Crossref | Google Scholar | PubMed |

Wang G, Qi K, Gao X, Guo L, Cao P, Li Q, Qiao X, Gu C, Zhang S (2022) Genome-wide identification and comparative analysis of the PYL gene family in eight Rosaceae species and expression analysis of seeds germination in pear. BMC Genomics 23(1), 233.
| Crossref | Google Scholar | PubMed |

Wang J, Chitsaz F, Derbyshire MK, Gonzales NR, Gwadz M, Lu S, Marchler GH, Song JS, Thank N, Yamashita RA, Yang M, Zhang D, Zheng C, Lanczycki CJ, Marchler-Bauer A (2023) The conserved domain database in 2023. Nucleic Acids Research 51(D1), D384-D388.
| Crossref | Google Scholar | PubMed |

Wang Z, Zhou J, Zou J, Yang J, Chen W (2024) Characterization of PYL gene family and identification of HaPYL genes response to drought and salt stress in sunflower. PeerJ 12, e16831.
| Crossref | Google Scholar | PubMed |

Wu X, Zhu J, Chen X, Zhang J, Lu L, Hao Z, Shi J, Chen J (2023) PYL family genes from Liriodendron chinense positively respond to multiple stresses. Plants 12, 2609.
| Crossref | Google Scholar | PubMed |

Yadav SK, Santosh Kumar VV, Verma RK, Yadav P, Saroha A, Wankhede DP, Chaudhary B, Chinnusamy V (2020) Genome-wide identification and characterization of ABA receptor PYL gene family in rice. BMC Genomics 21, 676.
| Crossref | Google Scholar |

Yanai I (2022) Quantifying gene duplication. Nature Reviews Genetics 23(4), 196-197.
| Crossref | Google Scholar | PubMed |

Yin K, Cheng F, Ren H, Huang J, Zhao X, Yuan Z (2024) Insights into the PYR/PYL/RCAR gene family in pomegranates (Punica granatum L.): a genome-wide study on identification, evolution, and expression analysis. Horticulturae 10(5), 502.
| Crossref | Google Scholar |

Zaidi F, Shahzad A, Ahsan M, Gul H, Shahzad M, Gul S, Mohamed S (2022) Evaluation of genetic variation among maize inbred lines for salinity stress at seedling stage through salt-stress-responsive traits. Acta Universitatis Sapientiae, Agriculture and Environment 14(1), 62-84.
| Crossref | Google Scholar |

Zhang H, Fen X, Yu W, Hu H-H, Dai X-F (2017) Progress of potato staple food research and industry development in China. Journal of Integrative Agriculture 16(12), 2924-2932.
| Crossref | Google Scholar |

Zhang G, Tang R, Niu S, Si H, Yang Q, Rajora OP, Li X-Q (2021) Heat-stress-induced sprouting and differential gene expression in growing potato tubers: comparative transcriptomics with that induced by postharvest sprouting. Horticulture Research 8, 226.
| Crossref | Google Scholar |

Zhang Z, Luo S, Liu Z, Wan Z, Gao X, Qiao Y, Yu J, Zhang G (2022a) Genome-wide identification and expression analysis of the cucumber PYL gene family. PeerJ 10, e12786.
| Crossref | Google Scholar | PubMed |

Zhang H, Zhu J, Gong Z, Zhu J-K (2022b) Abiotic stress responses in plants. Nature Reviews Genetics 23(2), 104-119.
| Crossref | Google Scholar | PubMed |

Zhang F, Yang J, Zhang N, Wu J, Si H (2022c) Roles of microRNAs in abiotic stress response and characteristics regulation of plant. Frontiers in Plant Science 13, 919243.
| Crossref | Google Scholar | PubMed |

Zhao Y, Chan Z, Gao J, Xing L, Cao M, Yu C, Hu Y, You J, Shi H, Zhu Y, Gong Y, Mu Z, Wang H, Deng X, Wang P, Bressan RA, Zhu J-K (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proceedings of the National Academy of Sciences 113(7), 1949-1954.
| Crossref | Google Scholar |

Zhao H, Nie K, Zhou H, Yan X, Zhan Q, Zheng Y, Song C-P (2020) ABI5 modulates seed germination via feedback regulation of the expression of the PYR/PYL/RCAR ABA receptor genes. New Phytologist 228(2), 596-608.
| Crossref | Google Scholar | PubMed |

Zhou J, An F, Sun Y, Guo R, Pan L, Wan T, Hao Y, Cai Y (2023) Genome-wide identification of the ABA receptor PYL gene family and expression analysis in Prunus avium L. Scientia Horticulturae 313, 111919.
| Crossref | Google Scholar |

Zhu L, Yan K, Ren J, Chen Z, Ma Q, Du Y, Wang Y, Li S, Li Q (2024) Genome-wide investigation of the PYL genes in Acer palmatum and their role in freezing tolerance. Industrial Crops and Products 210, 118107.
| Crossref | Google Scholar |

Zuo Z-F, He W, Li J, Mo B, Liu L (2021) Small RNAs: the essential regulators in plant thermotolerance. Frontiers in Plant Science 12, 726762.
| Crossref | Google Scholar | PubMed |