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RESEARCH ARTICLE

Transcriptome analysis of maize pollen grains under drought stress during flowering

Yinping Zhang A B , Soualiou Soualihou A C , Juan Li D , Yonghan Xu A , Ray J. Rose E , Yong-Ling Ruan E , Jincai Li A * and Youhong Song https://orcid.org/0000-0001-7163-149X A F *
+ Author Affiliations
- Author Affiliations

A School of Agronomy, Anhui Agricultural University, Hefei, Anhui Province 230036, China.

B Crop Research Institute, Anhui Academy of Agricultural Sciences, Hefei, Anhui Province 230031, China.

C Present address: Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China.

D Rice Research Institute, Anhui Academy of Agricultural Sciences, Hefei, Anhui Province 230031, China.

E School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia.

F Centre for Crop Science, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, Qld 4072, Australia.

* Correspondence to: ljc5122423@126.com, uqysong@163.com

Handling Editor: Enrico Francia

Crop & Pasture Science 73(9) 1026-1041 https://doi.org/10.1071/CP21610
Submitted: 29 July 2021  Accepted: 4 January 2022   Published: 11 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Drought stress is detrimental to male reproduction in maize (Zea mays L.), largely through reducing the quantity and quality of pollen grains. However, transcriptional response of maize pollen grains to drought stress has not been well documented. We compared pollen gene expression for a maize hybrid (ZhongDan909) under well-watered and drought-stress conditions, based on RNA-Seq validated by quantitative real-time PCR analysis. Expression of 6424 genes and 1302 transcripts was altered in pollen grains of maize subjected to 7 days of drought during flowering. Gene Ontology annotations showed 308 differentially expressed genes, annotated and classified into 50 primary functional categories. Kyoto Encyclopedia of Genes and Genomes analyses revealed 44 differentially expressed genes in nine metabolic pathways. In relation to carbohydrate metabolism pathways, there was downregulation of a polygalacturonase gene, which could reduce cell wall lysis in early pollen germination, and an increase in callose synthase transcripts along with reduced cellulase transcripts. These altered gene expressions responsible for cell wall integrity may inhibit the initiation of pollen tube growth. The onset of tube growth could be further impeded by observed changes in gene expression that potentially influence hormone metabolism (including downregulation of AUXIN RESPONSE FACTOR 18 and EIN3-BINDING F-BOX), reduce mitochondrial function, and alter protein translation. Genes with potential roles in adaptation were also altered in their transcript levels. These included genes encoding the upregulated transcription factor ZmNF-YC2, and the downregulated ZmbHLH13, a negative regulator of jasmonic acid responses. The upregulated flavin enzyme gene DIHYDROLIPOYL DEHYDROGENASE 1, associated with increased levels of reactive oxygen species, is of interest in relating redox homeostasis to stress adaptation. Overall, the analyses identified a suite of genes involved in the development of pollen grains and tubes and responsive to drought stress. The findings enhance understanding of the gene networks underlying compromised pollen viability under drought stress.

Keywords: anthesis, differentially expressed genes, drought stress, pollen development, pollen vitality, reporductive tissue, Zea mays L.


References

AbdElgawad H, Avramova V, Baggerman G, Van Raemdonck G, Valkenborg D, Van Ostade X, Guisez Y, Prinsen E, Asard H, Van den Ende W, Beemster GTS (2020) Starch biosynthesis contributes to the maintenance of photosynthesis and leaf growth under drought stress in maize. Plant, Cell & Environment 43, 2254–2271.
Starch biosynthesis contributes to the maintenance of photosynthesis and leaf growth under drought stress in maize.Crossref | GoogleScholarGoogle Scholar |

Allen RL, Lonsdale DM (1993) Molecular characterization of one of the maize polygalacturonase gene family members which are expressed during late pollen development. The Plant Journal 3, 261–271.
Molecular characterization of one of the maize polygalacturonase gene family members which are expressed during late pollen development.Crossref | GoogleScholarGoogle Scholar | 8106080PubMed |

Andrade FH, Vega C, Uhart S, Cirilo A, Cantarero M, Valentinuz O (1999) Kernel number determination in maize. Crop Science 39, 453–459.
Kernel number determination in maize.Crossref | GoogleScholarGoogle Scholar |

Aslam M, Maqbool MA, Cengiz R (2015) ‘Drought stress in maize (Zea mays L.): effects, resistance mechanisms, global achievements and biological strategies for improvement.’ Springer Briefs in Agriculture. (Springer Nature: Cham, Switzerland)
| Crossref |

Babujee L, Wurtz V, Ma C, Lueder F, Soni P, Van Dorsselaer A, Reumann S (2010) The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes. Journal of Experimental Botany 61, 1441–1453.
The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes.Crossref | GoogleScholarGoogle Scholar | 20150517PubMed |

Baldoni E, Genga A, Cominelli E (2015) Plant MYB transcription factors: their role in drought response mechanisms. International Journal of Molecular Sciences 16, 15811–15851.
Plant MYB transcription factors: their role in drought response mechanisms.Crossref | GoogleScholarGoogle Scholar | 26184177PubMed |

Bechtold U, Albihlal WS, Lawson T, Fryer MJ, Sparrow PAC, Richard F (2013) Arabidopsis HEAT SHOCK TRANSCRIPTION FACTOR1b overexpression enhances water productivity, resistance to drought, and infection. Journal of Experimental Botany 64, 3467–3481.
Arabidopsis HEAT SHOCK TRANSCRIPTION FACTOR1b overexpression enhances water productivity, resistance to drought, and infection.Crossref | GoogleScholarGoogle Scholar | 23828547PubMed |

Bérczi A, Møller IM (2000) Redox enzymes in the plant plasma membrane and their possible roles. Plant, Cell & Environment 23, 1287–1302.
Redox enzymes in the plant plasma membrane and their possible roles.Crossref | GoogleScholarGoogle Scholar |

Borg AJE, Dennig A, Weber H, Nidetzky B (2021) Mechanistic characterization of UDP-glucuronic acid 4-epimerase. The FEBS Journal 228, 1163–1178.
Mechanistic characterization of UDP-glucuronic acid 4-epimerase.Crossref | GoogleScholarGoogle Scholar |

Cascallares M, Setzes N, Marchetti F, López GA, Distéfano AM, Cainzos M, Zabaleta E, Pagnussat GC (2020) A complex journey: cell wall remodeling, interactions, and integrity during pollen tube growth. Frontiers in Plant Science 11, 599247
A complex journey: cell wall remodeling, interactions, and integrity during pollen tube growth.Crossref | GoogleScholarGoogle Scholar | 33329663PubMed |

Chen XY, Kim JY (2009) Callose synthesis in higher plants. Plant Signaling & Behavior 4, 489–492.
Callose synthesis in higher plants.Crossref | GoogleScholarGoogle Scholar |

Chen Y, Chen Y, Shi Z, Jin Y, Sun H, Xie F, Zhang L (2019) Biosynthesis and signal transduction of ABA, JA, and BRs in response to drought stress of Kentucky Bluegrass. International Journal of Molecular Sciences 20, 1289
Biosynthesis and signal transduction of ABA, JA, and BRs in response to drought stress of Kentucky Bluegrass.Crossref | GoogleScholarGoogle Scholar |

Dai S, Chen T, Chong K, Xue Y, Liu S, Wang T (2007) Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Molecular & Cellular Proteomics 6, 207–230.
Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen.Crossref | GoogleScholarGoogle Scholar |

Danilevskaya ON, Yu GX, Meng X, Xu J, Stephenson E, Estrada S, Chilakamarri S, Zastrow-Hayes G, Thatcher S (2019) Developmental and transcriptional responses of maize to drought stress under field conditions. Plant Direct 3, e00129
Developmental and transcriptional responses of maize to drought stress under field conditions.Crossref | GoogleScholarGoogle Scholar | 31245774PubMed |

Davidson RM, Hansey CN, Malali G, Childs KL, Haining L, Brieanne V, et al. (2011) Utility of RNA sequencing for analysis of maize reproductive transcriptomes. The Plant Genome 4, 191–203.
Utility of RNA sequencing for analysis of maize reproductive transcriptomes.Crossref | GoogleScholarGoogle Scholar |

Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. The Plant Journal 42, 315–328.
Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15842618PubMed |

Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17, 1866–1875.
Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses.Crossref | GoogleScholarGoogle Scholar | 15987996PubMed |

Frazee AC, Pertea G, Jaffe AE, Langmead B, Salzberg SL, Leek JT (2015) Ballgown bridges the gap between transcriptome assembly and expression analysis. Nature Biotechnology 33, 243–246.
Ballgown bridges the gap between transcriptome assembly and expression analysis.Crossref | GoogleScholarGoogle Scholar | 25748911PubMed |

Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo SD, Yanagisawa S, Vierstra RD (2004) Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proceedings of the National Academy of Sciences of the United States of America 101, 6803–6808.
Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation.Crossref | GoogleScholarGoogle Scholar | 15090654PubMed |

Gao C, Wang Y, Qu H (2019) Study of auxin regulation of pollen tube growth through calcium channels in Pyrus pyrifolia. Plant Growth Regulation 89, 99–108.
Study of auxin regulation of pollen tube growth through calcium channels in Pyrus pyrifolia.Crossref | GoogleScholarGoogle Scholar |

Geng X, Ye J, Yang X, Li S, Zhang L, Song X (2018) Identification of proteins involved in carbohydrate metabolism and energy metabolism pathways and their regulation of cytoplasmic male sterility in wheat. International Journal of Molecular Sciences 19, 324
Identification of proteins involved in carbohydrate metabolism and energy metabolism pathways and their regulation of cytoplasmic male sterility in wheat.Crossref | GoogleScholarGoogle Scholar |

Gong F, Wu X, Wang W (2015) Diversity and function of maize pollen coat proteins: from biochemistry to proteomics. Frontiers in Plant Science 6, 199
Diversity and function of maize pollen coat proteins: from biochemistry to proteomics.Crossref | GoogleScholarGoogle Scholar | 25870606PubMed |

Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5, 4864–4884.
Proteome mapping of mature pollen of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 16247729PubMed |

Hong E, Lim CW, Han SW, Lee SC (2017) Functional analysis of the pepper ethylene-responsive transcription factor, CaAIEF1, in enhanced ABA sensitivity and drought tolerance. Frontiers in Plant Science 8, 1407
Functional analysis of the pepper ethylene-responsive transcription factor, CaAIEF1, in enhanced ABA sensitivity and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 28878786PubMed |

Humbert S, Subedi S, Cohn J, Zeng B, Bi YM, Chen X, et al. (2013) Genome-wide expression profiling of maize in response to individual and combined water and nitrogen stresses. BMC Genomics 14, 3
Genome-wide expression profiling of maize in response to individual and combined water and nitrogen stresses.Crossref | GoogleScholarGoogle Scholar | 23324127PubMed |

Iaria D, Chiappetta A, Muzzalupo I (2016) De novo transcriptome sequencing of Olea europaea L. to identify genes involved in the development of the pollen tube. The Scientific World Journal 2016, 4305252
De novo transcriptome sequencing of Olea europaea L. to identify genes involved in the development of the pollen tube.Crossref | GoogleScholarGoogle Scholar | 26998509PubMed |

Ilyas N, Gull R, Mazhar R, Saeed M, Kanwal S, Shabir S, Bibi F (2017) Influence of salicylic acid and jasmonic acid on wheat under drought stress. Communications in Soil Science and Plant Analysis 48, 2715–2723.
Influence of salicylic acid and jasmonic acid on wheat under drought stress.Crossref | GoogleScholarGoogle Scholar |

Jain M (2011) Next-generation sequencing technologies for gene expression profiling in plants. Briefings in Functional Genomics 11, 63–70.
Next-generation sequencing technologies for gene expression profiling in plants.Crossref | GoogleScholarGoogle Scholar | 22155524PubMed |

Jegadeesan S, Chaturvedi P, Ghatak A, Pressman E, Meir S, Faigenboim A, Rutley N, Beery A, Harel A, Weckwerth W, Firon N (2018) Proteomics of heat-stress and ethylene-mediated thermotolerance mechanisms in tomato pollen grains. Frontiers in Plant Science 9, 1558
Proteomics of heat-stress and ethylene-mediated thermotolerance mechanisms in tomato pollen grains.Crossref | GoogleScholarGoogle Scholar | 30483278PubMed |

Jia H, Yang J, Liesche J, Liu X, Hu Y, Si W, Guo J, Li J (2018) Ethylene promotes pollen tube growth by affecting acting filament organization via the cGMP-dependent pathway in Arabidopsis thaliana. Protoplasma 255, 273–284.
Ethylene promotes pollen tube growth by affecting acting filament organization via the cGMP-dependent pathway in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 28864968PubMed |

Jia S, Li H, Jiang Y, Tang Y, Zhao G, Zhang Y, Yang S, Qiu H, Wang Y, Guo J, Yang Q, Shao R (2020) Transcriptomic analysis of female panicles reveals gene expression responses to drought stress in maize (Zea mays L.). Agronomy 10, 313
Transcriptomic analysis of female panicles reveals gene expression responses to drought stress in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |

Kakumanu A, Ambavaram MMR, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiology 160, 846–867.
Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq.Crossref | GoogleScholarGoogle Scholar | 22837360PubMed |

Kim KH, Song K, Park JM, Kim JY, Lee BM (2021) RNA-Seq analysis of gene expression changes related to delay of flowering time under drought stress in tropical maize. Applied Sciences 11, 4273
RNA-Seq analysis of gene expression changes related to delay of flowering time under drought stress in tropical maize.Crossref | GoogleScholarGoogle Scholar |

Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2011) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnology Journal 9, 315–327.
Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance.Crossref | GoogleScholarGoogle Scholar | 20809928PubMed |

Li J, Foster R, Ma S, Liao S, Bliss S, Kartika D, Wang L, Wu L, Eamens AL, Ruan Y-L (2021) Identification of transcription factors controlling cell wall invertase gene expression for reproductive development via bioinformatic and transgenic analyses. The Plant Journal 106, 1058–1074.
Identification of transcription factors controlling cell wall invertase gene expression for reproductive development via bioinformatic and transgenic analyses.Crossref | GoogleScholarGoogle Scholar | 33650173PubMed |

Liao S, Wang L, Li L, Ruan Y-L (2020) Cell wall invertase is essential for ovule development through sugar signalling rather than provision of carbon nutrients. Plant Physiology 183, 1126–1144.
Cell wall invertase is essential for ovule development through sugar signalling rather than provision of carbon nutrients.Crossref | GoogleScholarGoogle Scholar | 32332089PubMed |

Liu Y, Li J, Zhu Y, Jones A, Rose RJ, Song Y (2019) Heat stress in legume seed setting: effects, causes, and future prospects. Frontiers in Plant Science 10, 938
Heat stress in legume seed setting: effects, causes, and future prospects.Crossref | GoogleScholarGoogle Scholar | 31417579PubMed |

Liu S, Li C, Wang H, Wang S, Yang S, Liu X, Yan J, Li B, Beatty M, Zastrow-Hayes G, Song S, Qin F (2020) Mapping regulatory variants controlling gene expression in drought response and tolerance in maize. Genome Biology 21, 163
Mapping regulatory variants controlling gene expression in drought response and tolerance in maize.Crossref | GoogleScholarGoogle Scholar | 32631406PubMed |

Lobell DB, Roberts MJ, Schlenker W, Braun N, Little BB, Rejesus RM, Hammer GL (2014) Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest. Science 344, 516–519.
Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest.Crossref | GoogleScholarGoogle Scholar | 24786079PubMed |

Luo T, Zou T, Yuan G, He Z, Li W, Tao Y, Liu M, Zhou D, Zhao H, Zhu J, Liang Y, Deng Q, Wang S, Zheng A, Liu H, Wang L, Li P, Li S (2020) Less and shrunken pollen 1 (LSP1) encodes a member of the ABC transporter family required for pollen wall development in rice (Oryza sativa L.). The Crop Journal 8, 492–504.
Less and shrunken pollen 1 (LSP1) encodes a member of the ABC transporter family required for pollen wall development in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Lurin C, Andreés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette M-L, Mireau H, Peeters N, Renou J-P, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. The Plant Cell 16, 2089–2103.
Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis.Crossref | GoogleScholarGoogle Scholar | 15269332PubMed |

Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21, 3787–3793.
Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary.Crossref | GoogleScholarGoogle Scholar | 15817693PubMed |

Masiero S, Colombo L, Grini PE, Schnittger A, Kater MM (2011) The emerging importance of type I MADS box transcription factors for plant reproduction. The Plant Cell 23, 865–872.
The emerging importance of type I MADS box transcription factors for plant reproduction.Crossref | GoogleScholarGoogle Scholar | 21378131PubMed |

Miao Z, Han Z, Zhang T, Chen S, Ma C (2017) A systems approach to a spatio-temporal understanding of the drought stress response in maize. Scientific Reports 7, 6590
A systems approach to a spatio-temporal understanding of the drought stress response in maize.Crossref | GoogleScholarGoogle Scholar | 28747711PubMed |

Min H, Chen C, Wei S, Shang X, Sun M, Xia R, Liu X, Hao D, Chen H, Xie Q (2016) Identification of drought-tolerant mechanisms in maize seedlings based on transcriptome analysis of recombination inbred lines. Frontiers in Plant Science 7, 1080
Identification of drought-tolerant mechanisms in maize seedlings based on transcriptome analysis of recombination inbred lines.Crossref | GoogleScholarGoogle Scholar | 27507977PubMed |

Mittler R, Vanderauwera S, Suzuki N, Miller GAD, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends in Plant Science 16, 300–309.
ROS signaling: the new wave?Crossref | GoogleScholarGoogle Scholar | 21482172PubMed |

Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, Hinchey BS, Kumimoto RW, Maszle DR, Canales RD, Krolikowski KA, Dotson SB, Gutterson N, Ratcliffe OJ, Heard JE (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Sciences of the United States of America 104, 16450–16455.
Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres.Crossref | GoogleScholarGoogle Scholar | 17923671PubMed |

Parre E, Geitmann A (2005) More than a leak sealant. The mechanical properties of callose in pollen tubes. Plant Physiology 137, 274–286.
More than a leak sealant. The mechanical properties of callose in pollen tubes.Crossref | GoogleScholarGoogle Scholar | 15618431PubMed |

Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology 33, 290–295.
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads.Crossref | GoogleScholarGoogle Scholar | 25690850PubMed |

Piršelová B, Matušíková I (2013) Callose: the plant cell wall polysaccharide with multiple biological functions. Acta Physiologiae Plantarum 35, 635–644.
Callose: the plant cell wall polysaccharide with multiple biological functions.Crossref | GoogleScholarGoogle Scholar |

Poroyko V, Spollen WG, Hejlek LG, Hernandez AG, LeNoble ME, Davis G, et al. (2007) Comparing regional transcript profiles from maize primary roots under well-watered and low water potential conditions. Journal of Experimental Botany 58, 279–289.
Comparing regional transcript profiles from maize primary roots under well-watered and low water potential conditions.Crossref | GoogleScholarGoogle Scholar | 16990373PubMed |

Portwood JL, Woodhouse MR, Cannon EK, Gardiner JM, Harper LC, Schaeffer ML, Walsh JR, Sen TZ, Cho KT, Schott DA, Braun BL, Dietze M, Dunfee B, Elsik CG, Manchanda N, Coe E, Sachs M, Stinard P, Tolbert J, Zimmerman S, Andorf CM (2019) MaizeGDB 2018: The maize multi-genome genetics and genomics database. Nucleic Acids Research 47, D1146–D1154.
MaizeGDB 2018: The maize multi-genome genetics and genomics database.Crossref | GoogleScholarGoogle Scholar | 30407532PubMed |

Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran L-SP, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant Journal 50, 54–69.
Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L.Crossref | GoogleScholarGoogle Scholar |

Rigoulet M, Yoboue ED, Devin A (2011) Mitochondrial ROS generation and its regulation: mechanisms involved in H2O2 signaling. Antioxidants & Redox Signaling 14, 459–468.
Mitochondrial ROS generation and its regulation: mechanisms involved in H2O2 signaling.Crossref | GoogleScholarGoogle Scholar |

Rose RJ, Sheahan MB (2012) Plant mitochondria. In ‘Encyclopedia of life sciences (eLS)’. (John Wiley & Sons, Ltd: Chichester, UK)
| Crossref |

Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Molecular Plant 3, 942–955.
Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat.Crossref | GoogleScholarGoogle Scholar | 20729475PubMed |

Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends in Plant Science 17, 656–665.
Molecular regulation of seed and fruit set.Crossref | GoogleScholarGoogle Scholar | 22776090PubMed |

Schussler JR, Westgate ME (1995) Assimilate flux determines kernel set at low water potential in maize. Crop Science 35, 1074–1080.
Assimilate flux determines kernel set at low water potential in maize.Crossref | GoogleScholarGoogle Scholar |

Seale M (2020) Callose deposition during pollen development. Plant Physiology 184, 564–565.
Callose deposition during pollen development.Crossref | GoogleScholarGoogle Scholar | 33020323PubMed |

Shen S, Ma S, Liu YH, Liao SJ, Li J, Kartika D, Wu LM, Mock H-P, Ruan Y-L (2019) Cell wall invertase and sugar transporters are differentially activated in tomato styles and ovaries during pollination and fertilization. Frontiers in Plant Science 10, 506
Cell wall invertase and sugar transporters are differentially activated in tomato styles and ovaries during pollination and fertilization.Crossref | GoogleScholarGoogle Scholar | 31057596PubMed |

Shin S, Ju S L, Sang GK, Go TH, Shon J, Kang S, et al. (2015) Yield of maize (Zea mays L.) logistically declined with increasing length of the consecutive visible wilting days during flowering. Journal of Crop Science and Biotechnology 18, 237–248.
Yield of maize (Zea mays L.) logistically declined with increasing length of the consecutive visible wilting days during flowering.Crossref | GoogleScholarGoogle Scholar |

Somaratne Y, Tian Y, Zhang H, Wang M, Huo Y, Cao F, Zhao L, Chen H (2017) Abnormal Pollen Vacuolation1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize. The Plant Journal 90, 96–110.
Abnormal Pollen Vacuolation1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize.Crossref | GoogleScholarGoogle Scholar | 28078801PubMed |

Song Y, Birch C, Qu S, Hanan J (2010) Analysis and modelling of the effects of water stress on maize growth and yield in dryland conditions. Plant Production Science 13, 199–208.
Analysis and modelling of the effects of water stress on maize growth and yield in dryland conditions.Crossref | GoogleScholarGoogle Scholar |

Song S, Qi T, Fan M, Zhang X, Gao H, Huang H, Wu D, Guo H, Xie D (2013) The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development. PLoS Genetics 9, e1003653
The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development.Crossref | GoogleScholarGoogle Scholar | 23935516PubMed |

Song K, Kim HC, Shin S, Kim K-H, Moon JC, Kim JY, Lee BM (2017) Transcriptome analysis of flowering time genes under drought stress in maize leaves. Frontiers in Plant Science 8, 267
Transcriptome analysis of flowering time genes under drought stress in maize leaves.Crossref | GoogleScholarGoogle Scholar | 28298916PubMed |

Timm S, Wittmiß M, Gamlien S, Ewald R, Florian A, Frank M, Wirtz M, Hell R, Fernie AR, Bauwe H (2015) Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. The Plant Cell 27, 1968–1984.
Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 26116608PubMed |

Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28, 511–515.
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.Crossref | GoogleScholarGoogle Scholar | 20436464PubMed |

Wang J, Wang CY (2021) Integrated miRNA and mRNA omics reveal the anti-cancerous mechanism of Licochalcone B on Human Hepatoma Cell HepG2. Food and Chemical Toxicology 150, 112096
Integrated miRNA and mRNA omics reveal the anti-cancerous mechanism of Licochalcone B on Human Hepatoma Cell HepG2.Crossref | GoogleScholarGoogle Scholar | 33647349PubMed |

Wang B, Liu C, Zhang D, He C, Zhang J, Li Z (2019) Effects of maize organ-specific drought stress response on yields from transcriptome analysis. BMC Plant Biology 19, 335
Effects of maize organ-specific drought stress response on yields from transcriptome analysis.Crossref | GoogleScholarGoogle Scholar | 31370805PubMed |

Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellins and other hormones. Plant Physiology 144, 1240–1246.
Mechanisms of cross talk between gibberellins and other hormones.Crossref | GoogleScholarGoogle Scholar | 17616507PubMed |

Wu JZ, Lin Y, Zhang XL, Pang DW, Zhao J (2008) IAA stimulates pollen tube growth and mediates the modification of its wall composition and structure in Torenia fournieri. Journal of Experimental Botany 59, 2529–2543.
IAA stimulates pollen tube growth and mediates the modification of its wall composition and structure in Torenia fournieri.Crossref | GoogleScholarGoogle Scholar | 18544613PubMed |

Wu Z, Cheng J, Qin C, Hu Z, Yin C, Hu K (2013) Differential proteomic analysis of anthers between cytoplasmic male sterile and maintainer lines in Capsicum annuum L. International Journal of Molecular Sciences 14, 22982–22996.
Differential proteomic analysis of anthers between cytoplasmic male sterile and maintainer lines in Capsicum annuum L.Crossref | GoogleScholarGoogle Scholar | 24264042PubMed |

Xing H, Pudake RN, Guo G, Xing G, Hu Z, Zhang Y, Sun Q, Ni Z (2011) Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics 12, 178
Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize.Crossref | GoogleScholarGoogle Scholar | 21473768PubMed |

Yan X, Dong C, Yu J, Liu W, Jiang C, Liu J, Hu Q, Fang X, Wei W (2013) Transcriptome profile analysis of young floral buds of fertile and sterile plants from the self-pollinated offspring of the hybrid between novel restorer line NR1 and Nsa CMS line in Brassica napus. BMC Genomics 14, 26
Transcriptome profile analysis of young floral buds of fertile and sterile plants from the self-pollinated offspring of the hybrid between novel restorer line NR1 and Nsa CMS line in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 23324545PubMed |

Yang J, Tian L, Sun MX, Huang XY, Zhu J, Guan YF, Jia QS, Yang ZN (2013) AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiology 162, 720–731.
AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23580594PubMed |

Yang K, Zhou X, Wang Y, Feng H, Ren X, Liu H, Liu W (2017) Carbohydrate metabolism and gene regulation during anther development in an androdioecious tree, Tapiscia sinensis. Annals of Botany 120, 967–977.
Carbohydrate metabolism and gene regulation during anther development in an androdioecious tree, Tapiscia sinensis.Crossref | GoogleScholarGoogle Scholar | 28961748PubMed |

Zenda T, Liu S, Wang X, Liu G, Jin H, Dong A, Yang Y, Duan H (2019) Key maize drought-responsive genes and pathways revealed by comparative transcriptome and physiological analyses of contrasting inbred lines. International Journal of Molecular Sciences 20, 1268
Key maize drought-responsive genes and pathways revealed by comparative transcriptome and physiological analyses of contrasting inbred lines.Crossref | GoogleScholarGoogle Scholar |

Zhang L, Liu H, Sun J, Li J, Song Y (2018) Seedling characteristics and grain yield of maize grown under straw retention affected by sowing irrigation and splitting nitrogen use. Field Crops Research 225, 22–31.
Seedling characteristics and grain yield of maize grown under straw retention affected by sowing irrigation and splitting nitrogen use.Crossref | GoogleScholarGoogle Scholar |

Zheng J, Fu J, Gou M, Huai J, Liu Y, Jian M, Huang Q, Guo X, Dong Z, Wang H, Wang G (2010) Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Molecular Biology 72, 407–421.
Genome-wide transcriptome analysis of two maize inbred lines under drought stress.Crossref | GoogleScholarGoogle Scholar | 19953304PubMed |

Zhu J, Yang ZN (2013) The research progress of pollen wall development. Chinese Journal of Nature 35, 112–117.
The research progress of pollen wall development.Crossref | GoogleScholarGoogle Scholar |