A Systematic Investigation of Lipid Transfer Proteins Involved in Male Fertility and Other Biological Processes in Maize

Plant lipid transfer proteins (LTPs) play essential roles in various biological processes, including anther and pollen development, vegetative organ development, seed development and germination, and stress response, but the research progress varies greatly among Arabidopsis, rice and maize. Here, we presented a preliminary introduction and characterization of the whole 65 LTP genes in maize, and performed a phylogenetic tree and gene ontology analysis of the LTP family members in maize. We compared the research progresses of the reported LTP genes involved in male fertility and other biological processes in Arabidopsis and rice, and thus provided some implications for their maize orthologs, which will provide useful clues for the investigation of LTP transporters in maize. We predicted the functions of LTP genes based on bioinformatic analyses of their spatiotemporal expression patterns by using RNA-seq and qRT-PCR assays. Finally, we discussed the advances and challenges in substrate identification of plant LTPs, and presented the future research directions of LTPs in plants. This study provides a basic framework for functional research and the potential application of LTPs in multiple plants, especially for male sterility research and application in maize.

[1]  Xiangyuan Wan,et al.  Triphasic regulation of ZmMs13 encoding an ABCG transporter is sequentially required for callose dissolution, pollen exine and anther cuticle formation in maize , 2022, Journal of advanced research.

[2]  Xiangyuan Wan,et al.  The Bibliometric Landscape of Gene Editing Innovation and Regulation in the Worldwide , 2022, Cells.

[3]  Xiangyuan Wan,et al.  The ZmMYB84‐ZmPKSB regulatory module controls male fertility through modulating anther cuticle—pollen exine trade‐off in maize anthers , 2022, Plant biotechnology journal.

[4]  Yanbo Wang,et al.  ATP-Binding Cassette G Transporters and Their Multiple Roles Especially for Male Fertility in Arabidopsis, Rice and Maize , 2022, International journal of molecular sciences.

[5]  Yunhai Li,et al.  A natural allele of OsMS1 responds to temperature changes and confers thermosensitive genic male sterility , 2022, Nature communications.

[6]  Yaoguang Liu,et al.  OsLTP47 may function in a lipid transfer relay essential for pollen wall development in rice. , 2022, Journal of genetics and genomics = Yi chuan xue bao.

[7]  Xiangyuan Wan,et al.  Use of CRISPR/Cas9-Based Gene Editing to Simultaneously Mutate Multiple Homologous Genes Required for Pollen Development and Male Fertility in Maize , 2022, Cells.

[8]  G. Feng,et al.  Lipid transporter LSR1 positively regulates leaf senescence in Arabidopsis , 2021, Plant signaling & behavior.

[9]  Xiangyuan Wan,et al.  The essential roles of sugar metabolism for pollen development and male fertility in plants , 2021, The Crop Journal.

[10]  Shuangcheng Li,et al.  Secretory lipid transfer protein OsLTPL94 acts as a target of EAT1 and is required for rice pollen wall development. , 2021, The Plant journal : for cell and molecular biology.

[11]  Xiangyuan Wan,et al.  ZmFAR1 and ZmABCG26 Regulated by microRNA Are Essential for Lipid Metabolism in Maize Anther , 2021, International journal of molecular sciences.

[12]  Min-Shup Song,et al.  Comprehensive Transcriptome Analysis of Rare Carpinus putoensis Plants under NO2 stress , 2021, Genes.

[13]  Yanbo Wang,et al.  ZmMs25 Is Critical for Anther and Pollen Development in Maize. , 2021, Journal of experimental botany.

[14]  W. He,et al.  CRISPR/Cas9‐based discovery of maize transcription factors regulating male sterility and their functional conservation in plants , 2021, Plant biotechnology journal.

[15]  Xiang Li,et al.  Breeding with Dominant Genic Male-Sterility Genes to Boost Crop Grain Yield in Post-Heterosis Utilization Era. , 2021, Molecular plant.

[16]  Zheng Wang,et al.  A functional characterization of TaMs1 orthologs in Poaceae plants , 2021 .

[17]  T. Ovchinnikova,et al.  Interaction between the Lentil Lipid Transfer Protein Lc-LTP2 and Its Novel Signal Ligand PI(4,5)P2 , 2020, Membranes.

[18]  S. Persson,et al.  Grass-Specific EPAD1 Is Essential for Pollen Exine Patterning in Rice[OPEN] , 2020, Plant Cell.

[19]  W. Jin,et al.  Normal Structure and Function of Endothecium Chloroplasts Maintained by ZmMs33-mediated Lipid Biosynthesis in Tapetal Cells Are Critical for Anther Development in Maize. , 2020, Molecular plant.

[20]  Longping Yuan,et al.  Molecular regulation of ZmMs7 required for maize male fertility and development of a dominant male-sterility system in multiple species , 2020, Proceedings of the National Academy of Sciences.

[21]  R. Raina,et al.  An Arabidopsis DISEASE RELATED NONSPECIFIC LIPID TRANSFER PROTEIN 1 is required for resistance against various phytopathogens and tolerance to salt stress. , 2020, Gene.

[22]  Xiangyuan Wan,et al.  Lipid Metabolism: Critical Roles in Male Fertility and Other Aspects of Reproductive Development in Plants. , 2020, Molecular plant.

[23]  Jinfeng Chen,et al.  Genome-wide analysis of putative lipid transfer protein LTP_2 gene family reveals CsLTP_2 genes involved in response of cucumber against root-knot nematode (Meloidogyne incognita). , 2020, Genome.

[24]  Yaoguang Liu,et al.  A lipid transfer protein variant with a mutant eight-cysteine motif causes photoperiod- and thermo-sensitive dwarfism in rice , 2019, Journal of experimental botany.

[25]  Elizabeth A. Ainsworth,et al.  Genetic strategies for improving crop yields , 2019, Nature.

[26]  Shanshan Wang,et al.  The lipid transfer protein OsLTPL159 is involved in cold tolerance at the early seedling stage in rice , 2019, Plant biotechnology journal.

[27]  B. Arredondo-Vega,et al.  Involvement of OpsLTP1 from Opuntia streptacantha in abiotic stress adaptation and lipid metabolism. , 2019, Functional plant biology : FPB.

[28]  M. Tester,et al.  Breeding crops to feed 10 billion , 2019, Nature Biotechnology.

[29]  Xiangyuan Wan,et al.  Genome-wide analysis of maize GPAT gene family and cytological characterization and breeding application of ZmMs33/ZmGPAT6 gene , 2019, Theoretical and Applied Genetics.

[30]  Xiangyuan Wan,et al.  Maize Genic Male-Sterility Genes and Their Applications in Hybrid Breeding: Progress and Perspectives. , 2019, Molecular plant.

[31]  Yanbo Wang,et al.  ZmMs30 Encoding a Novel GDSL Lipase Is Essential for Male Fertility and Valuable for Hybrid Breeding in Maize. , 2019, Molecular plant.

[32]  D. Funck,et al.  Proline synthesis in developing microspores is required for pollen development and fertility , 2018, BMC Plant Biology.

[33]  W. Jin,et al.  Maize male sterile 33 encodes a putative glycerol-3-phosphate acyltransferase that mediates anther cuticle formation and microspore development , 2018, BMC plant biology.

[34]  M. Suh,et al.  Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein 15 affects seed coat permeability in Arabidopsis. , 2018, The Plant journal : for cell and molecular biology.

[35]  T. Ovchinnikova,et al.  Plant Pathogenesis-Related Proteins Binding Lipids and Other Hydrophobic Ligands , 2018, Russian Journal of Bioorganic Chemistry.

[36]  T. Levine,et al.  Lipid transfer proteins: the lipid commute via shuttles, bridges and tubes , 2018, Nature Reviews Molecular Cell Biology.

[37]  K. Hanada Lipid transfer proteins rectify inter-organelle flux and accurately deliver lipids at membrane contact sites , 2018, Journal of Lipid Research.

[38]  T. Salminen,et al.  Plant lipid transfer proteins: are we finally closing in on the roles of these enigmatic proteins? , 2018, Journal of Lipid Research.

[39]  Xiangyuan Wan,et al.  Map-based cloning and characterization of Zea mays male sterility33 (ZmMs33) gene, encoding a glycerol-3-phosphate acyltransferase , 2018, Theoretical and Applied Genetics.

[40]  Liqun Rao,et al.  Construction of a multicontrol sterility system for a maize male‐sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD‐finger transcription factor , 2017, Plant biotechnology journal.

[41]  Hang He,et al.  Poaceae-specific MS1 encodes a phospholipid-binding protein for male fertility in bread wheat , 2017, Proceedings of the National Academy of Sciences.

[42]  T. Levine,et al.  Advances on the Transfer of Lipids by Lipid Transfer Proteins , 2017, Trends in biochemical sciences.

[43]  B. Payre,et al.  The Arabidopsis Lipid Transfer Protein 2 (AtLTP2) Is Involved in Cuticle-Cell Wall Interface Integrity and in Etiolated Hypocotyl Permeability , 2017, Front. Plant Sci..

[44]  Bo Shen,et al.  A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize , 2017, Plant biotechnology journal.

[45]  M. Riedel,et al.  The Nonspecific Lipid Transfer Protein AtLtpI-4 Is Involved in Suberin Formation of Arabidopsis thaliana Crown Galls1[OPEN] , 2016, Plant Physiology.

[46]  T. Salminen,et al.  Lipid transfer proteins: classification, nomenclature, structure, and function , 2016, Planta.

[47]  K. Mineev,et al.  A novel lipid transfer protein from the dill Anethum graveolens L.: isolation, structure, heterologous expression, and functional characteristics , 2016, Journal of peptide science : an official publication of the European Peptide Society.

[48]  Wenya Guo,et al.  LTP3 contributes to disease susceptibility in Arabidopsis by enhancing abscisic acid (ABA) biosynthesis. , 2015, Molecular plant pathology.

[49]  S. Jülke,et al.  Response of Arabidopsis thaliana Roots with Altered Lipid Transfer Protein (LTP) Gene Expression to the Clubroot Disease and Salt Stress , 2015, Plants.

[50]  M. Pinedo,et al.  On the role of a Lipid-Transfer Protein. Arabidopsis ltp3 mutant is compromised in germination and seedling growth. , 2015, Plant signaling & behavior.

[51]  X. Wang,et al.  A lipid transfer protein, OsLTPL36, is essential for seed development and seed quality in rice. , 2015, Plant science : an international journal of experimental plant biology.

[52]  F. Liu,et al.  Non-specific lipid transfer proteins in plants: presenting new advances and an integrated functional analysis. , 2015, Journal of experimental botany.

[53]  Xiaoying Li,et al.  Histone H2B Monoubiquitination Mediated by HISTONE MONOUBIQUITINATION1 and HISTONE MONOUBIQUITINATION2 Is Involved in Anther Development by Regulating Tapetum Degradation-Related Genes in Rice1[OPEN] , 2015, Plant Physiology.

[54]  K. Wei,et al.  Non-specific lipid transfer proteins in maize , 2014, BMC Plant Biology.

[55]  P. Langridge,et al.  Expression patterns and protein structure of a lipid transfer protein END1 from Arabidopsis , 2014, Planta.

[56]  Monika M. Edstam,et al.  Involvement of GPI-anchored lipid transfer proteins in the development of seed coats and pollen in Arabidopsis thaliana. , 2014, Physiologia plantarum.

[57]  Anant K. Menon,et al.  Lipid landscapes and pipelines in membrane homeostasis , 2014, Nature.

[58]  L. Schreiber,et al.  ABORTED MICROSPORES Acts as a Master Regulator of Pollen Wall Formation in Arabidopsis[C][W][OPEN] , 2014, Plant Cell.

[59]  O. Sellam,et al.  Two maize END-1 orthologs, BETL9 and BETL9like, are transcribed in a non-overlapping spatial pattern on the outer surface of the developing endosperm , 2014, Front. Plant Sci..

[60]  A. Pitzschke,et al.  Salt Stress in Arabidopsis: Lipid Transfer Protein AZI1 and Its Control by Mitogen-Activated Protein Kinase MPK3 , 2013, Molecular plant.

[61]  A. Huang,et al.  Abundant Type III Lipid Transfer Proteins in Arabidopsis Tapetum Are Secreted to the Locule and Become a Constituent of the Pollen Exine1[W][OPEN] , 2013, Plant Physiology.

[62]  B. Han,et al.  The rice OsLTP6 gene promoter directs anther-specific expression by a combination of positive and negative regulatory elements , 2013, Planta.

[63]  P. Carella,et al.  Long distance movement of DIR1 and investigation of the role of DIR1-like during systemic acquired resistance in Arabidopsis , 2013, Front. Plant Sci..

[64]  Xiaochun Ge,et al.  The rice OsDIL gene plays a role in drought tolerance at vegetative and reproductive stages , 2013, Plant Molecular Biology.

[65]  J. Fowler,et al.  A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. , 2013, Cell reports.

[66]  G. Ma,et al.  Isolation and Functional Analysis of ZmLTP3, a Homologue to Arabidopsis LTP3 , 2013, International journal of molecular sciences.

[67]  Dabing Zhang,et al.  EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice , 2013, Nature Communications.

[68]  Yaoguang Liu,et al.  Characterization and genetic mapping of a Photoperiod-sensitive dwarf 1 locus in rice (Oryza sativa L.) , 2013, Theoretical and Applied Genetics.

[69]  I. Hwang,et al.  Characterization of glycosylphosphatidylinositol-anchored lipid transfer protein 2 (LTPG2) and overlapping function between LTPG/LTPG1 and LTPG2 in cuticular wax export or accumulation in Arabidopsis thaliana. , 2012, Plant & cell physiology.

[70]  E. Kurczynska,et al.  Distribution of lipid transfer protein 1 (LTP1) epitopes associated with morphogenic events during somatic embryogenesis of Arabidopsis thaliana , 2012, Plant Cell Reports.

[71]  T. Salminen,et al.  Evolutionary history of the non-specific lipid transfer proteins. , 2011, Molecular plant.

[72]  T. Ariizumi,et al.  Genetic regulation of sporopollenin synthesis and pollen exine development. , 2011, Annual review of plant biology.

[73]  D. Klessig,et al.  Interconnection between Methyl Salicylate and Lipid-Based Long-Distance Signaling during the Development of Systemic Acquired Resistance in Arabidopsis and Tobacco1[W] , 2011, Plant Physiology.

[74]  C. Kieslich,et al.  A multifaceted study of stigma/style cysteine-rich adhesin (SCA)-like Arabidopsis lipid transfer proteins (LTPs) suggests diversified roles for these LTPs in plant growth and reproduction , 2010, Journal of experimental botany.

[75]  Dabing Zhang,et al.  OsC6, Encoding a Lipid Transfer Protein, Is Required for Postmeiotic Anther Development In Rice1[W][OA] , 2010, Plant Physiology.

[76]  Dabing Zhang,et al.  Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. , 2010, Journal of integrative plant biology.

[77]  Dabing Zhang,et al.  The ABORTED MICROSPORES Regulatory Network Is Required for Postmeiotic Male Reproductive Development in Arabidopsis thaliana[W][OA] , 2010, Plant Cell.

[78]  C. Kieslich,et al.  A Gain-of-Function Mutation of Arabidopsis Lipid Transfer Protein 5 Disturbs Pollen Tube Tip Growth and Fertilization[C][W] , 2009, The Plant Cell Online.

[79]  M. Matsuoka,et al.  Gibberellin Modulates Anther Development in Rice via the Transcriptional Regulation of GAMYB[W] , 2009, The Plant Cell Online.

[80]  Inhwan Hwang,et al.  Disruption of Glycosylphosphatidylinositol-Anchored Lipid Transfer Protein Gene Altered Cuticular Lipid Composition, Increased Plastoglobules, and Enhanced Susceptibility to Infection by the Fungal Pathogen Alternaria brassicicola1[W] , 2009, Plant Physiology.

[81]  W. Xie,et al.  Calmodulin binds to maize lipid transfer protein and modulates its lipids binding ability , 2008, The FEBS journal.

[82]  Moon Chul Kim,et al.  Cutin monomer induces expression of the rice OsLTP5 lipid transfer protein gene. , 2008, Journal of plant physiology.

[83]  Hong Ma,et al.  The Rice Tapetum Degeneration Retardation Gene Is Required for Tapetum Degradation and Anther Development[W] , 2006, The Plant Cell Online.

[84]  M. Delseny,et al.  Inducibility by pathogen attack and developmental regulation of the rice Ltp1 gene , 2002, Plant Molecular Biology.

[85]  K. Toriyama,et al.  Molecular characterization of rice genes specifically expressed in the anther tapetum , 1994, Plant Molecular Biology.

[86]  Xiaochun Ge,et al.  Resistance function of rice lipid transfer protein LTP110. , 2003, Journal of biochemistry and molecular biology.

[87]  J. Puck,et al.  Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency , 2002, Nature.

[88]  Lauga,et al.  Characterization of MZm3-3, a Zea mays tapetum-specific transcript. , 2000, Plant Science.

[89]  J. Kader LIPID-TRANSFER PROTEINS IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[90]  M. Delseny,et al.  Characterization of a rice gene coding for a lipid transfer protein. , 1994, Gene.

[91]  C. Somerville,et al.  A non-specific lipid transfer protein from Arabidopsis is a cell wall protein. , 1993, The Plant journal : for cell and molecular biology.

[92]  P. Shewry,et al.  Molecular evolution of the seed storage proteins of barley, rye and wheat. , 1985, Journal of molecular biology.