Abstract
In higher plants, NHL (NDR1/HIN1-like) genes play important roles in response to both biotic and abiotic stresses. However, their biological functions in plant growth and development are largely unknown. Previously, we identified an NHL6 gene from Arabidopsis. Overexpression of NHL6 inhibited seed germination under abiotic stress conditions. In this work, we demonstrate that NHL6 also has a function in seed development. Transgenic Arabidopsis plants overexpressing NHL6 produced shorter siliques and fewer seeds per silique, but increased seed size, leading to decreased seed yield per plant. Pollen viability and meiosis studies did not show any difference between wild type and transgenic plants. In a yeast-two-hybrid screening, a tubby-like F-box protein AtTLP11 was identified as a potential interacting protein of NHL6, which was negatively correlated with NHL6 expression. Our results reveal a critical role of NHL gene in the seed development and a possible connection between NHL and AtTLP families in plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122
Bao Y, Song WM, Jin YL et al (2014a) Characterization of Arabidopsis tubby-like proteins and redundant function of AtTLP3 and AtTLP9 in plant response to ABA and osmotic stress. Plant Mol Biol 86:471–483
Bao Y, Wang CT, Jiang CM et al (2014b) The tumor necrosis factor receptor-associated factor (TRAF)-like family protein seven in absentia 2 (SINA2) promotes drought tolerance in an ABA-dependent manner in Arabidopsis. New Phytol 202:174–187
Bao Y, Song WM, Pan J et al (2016a) Overexpression of the NDR1/HIN1-like gene NHL6 modifies seed germination in response to abscisic acid and abiotic stresses in Arabidopsis. PLoS ONE 11:e0148572
Bao Y, Song WM, Zhang HX (2016b) Role of Arabidopsis NHL family in ABA and stress response. Plant Signal Behav 11:e1180493
Bies-Ethève N, Gaubier-Comella P, Debures A et al (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67:107–124
Candat A, Paszkiewicz G, Neveu M et al (2014) The ubiquitous distribution of late embryogenesis abundant proteins across cell compartments in Arabidopsis offers tailored protection against abiotic stress. Plant Cell 26:3148–3166
Dörmanna P, Gopalan S, He SY, Benning C (2000) A gene family in Arabidopsis thaliana with sequence similarity to NDR1 and HIN1. Plant Physiol Biochem 38:789–796
Dure L, Chlan C (1981) Developmental biochemistry of cottonseed embryogenesis and germination: XII. Purification and properties of principal storage proteins. Plant Physiol 68:180–186
Hua Z, Vierstra R, Merchant S et al (2011) The cullin-ring ubiquitin-protein ligases. Annu Rev Plant Biol 62:299–334
Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118
Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371
Kovacs D, Kalmar E, Torok Z et al (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381–390
Lai CP, Lee CL, Chen PH et al (2004) Molecular analyses of the Arabidopsis TUBBY-like protein gene family. Plant Physiol 134:1586–1597
Nakayama K, Okawa K, Kakizaki T et al (2008) Evaluation of the protective activities of a late embryogenesis abundant (LEA) related protein, Cor15am, during various stresses in vitro. Biosci Biotechnol Biochem 72:1642–1645
Nonogaki H (2014) Seed dormancy and germination-emerging mechanisms and new hypotheses. Front Plant Sci 5:233
Pontier D, Gan SS, Amasino RM, Roby D, Lam E (1999) Markers for hypersensitive response and senescence show distinct patterns of expression. Plant Mol Biol 39:1243–1255
Rasband WS, ImageJ US National Institutes of Health, Bethesda, Maryland, USA, https://imagej.nih.gov/ij/, 1997–2018
Reitz MU, Bissue JK, Zocher K et al (2012) The subcellular localization of tubby-like proteins and participation in stress signaling and root colonization by the mutualist Piriformospora indica. Plant Physiol 160:349–364
Shao HB, Liang ZS, Shao MA (2005) LEA proteins in higher plants: structure, function, gene expression and regulation. Colloids Surf B 45:131–135
Singh S, Cornilescu CC, Tyler RC et al (2005) Solution structure of a late embryogenesis abundant protein (LEA14) from Arabidopsis thaliana, a cellular stress-related protein. Protein Sci 14:2601–2609
Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol 64:189–217
Sun K, Hunt K, Hauser BA (2004) Ovule abortion in Arabidopsis triggered by stress. Plant Physiol 135:2358–2367
Tang RJ, Liu H, Bao Y et al (2010) The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol Biol 74:367–380
Varet A, Parker J, Tornero P et al (2002) NHL25 and NHL3, two NDR1/HIN1-1ike genes in Arabidopsis thaliana with potential role(s) in plant defense. Mol Plant Microb Interact 15:608–616
Varet A, Hause B, Hause G et al (2003) The Arabidopsis NHL3 gene encodes a plasma membrane protein and its overexpression correlates with increased resistance to Pseudomonas syringae pv. tomato DC3000. Plant Physiol 132:2023–2033
Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397
Vilaine F, Kerchev P, Clement G et al (2013) Increased expression of a phloem membrane protein encoded by NHL26 alters phloem export and sugar partitioning in Arabidopsis. Plant Cell 25:1689–1708
Wang Y, Cheng Z, Huang J et al (2012) The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana. PLoS Genet 8:e1003039
Wang Y, Cheng Z, Lu P et al (2014) Molecular cell biology of male meiotic chromosomes and isolation of male meiocytes in Arabidopsis thaliana. Methods Mol Biol 1110:217–230
Yang J, Yan R, Roy A et al (2015a) The I-TASSER suite: protein structure and function prediction. Nat Methods 12:7–8
Yang Y, Tang RJ, Li B et al (2015b) Overexpression of a populus trichocarpa H+-pyrophosphatase gene PtVP1.1 confers salt tolerance on transgenic poplar. Tree Physiol 35:663–677
Zheng MS, Takahashi H, Miyazaki A et al (2004) Up-regulation of Arabidopsis thaliana NHL10 in the hypersensitive response to Cucumber mosaic virus infection and in senescing leaves is controlled by signalling pathways that differ in salicylate involvement. Planta 218:740–750
Zheng MS, Takahashi H, Miyazaki A, Yamaguchi K, Kusano T (2005) Identification of the cis-acting elements in Arabidopsis thaliana NHL10 promoter responsible for leaf senescence, the hypersensitive response against Cucumber mosaic virus infection, and spermine treatment. Plant Sci 168:415–422
Funding
This work was supported by the National Key Program on Transgenic Research [Grant No. 2018ZX08020002]; the National Key R & D Program of China [Grant No. 2016YFD0600106]; the National Natural Science Foundation of China [Grant No. 31870576]; the National Major Project of GMO New Species Cultivation [Grant No. 2016ZX08004-002-006]; The Modern Agricultural Industry Technology System Innovation Team of Shandong Province of China [Grant No. SDAIT-02-05]; and Comprehensive Surveys on Saline Lake Lithium and other New Energy Resources in the North Tibetan Plateau [Grant No. DD20160025].
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Song, Wm., Cheng, Zh., Guo, Xt. et al. Overexpression of NHL6 affects seed production in transgenic Arabidopsis plants. Plant Growth Regul 88, 41–47 (2019). https://doi.org/10.1007/s10725-019-00486-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-019-00486-2