Abstract
In plants, the plasma membrane H+-ATPase (HA) is considered to play a crucial role in regulating plant growth and respoding to environment stresses. Multiple paralogous genes encoding different isozymes of HA have been identified and characterized in several model plants, while limited information of the HA gene family is available to date for tomato. Here, we describe the molecular and expression features of eight HA-encoding genes (SlHA1-8) from tomato. All these genes are interrupted by multiple introns with conserved positions. SlHA1, 2, and 4 were widely expressed in all tissues, while SlHA5, 6, and 7 were almost only expressed in flowers. SlHA8, the transcripts of which were barely detectable under normal or nutrient-/salt-stress growth conditions, was strongly activated in arbuscular mycorrhizal (AM) fungal-colonized roots. Extreme lack of SlHA8 expression in M161, a mutant defective to AM fungal colonization, provided genetic evidence towards the dependence of its expression on AM symbiosis. A 1521-bp SlHA8 promoter could direct the GUS reporter expression specifically in colonized cells of transgenic tobacco, soybean, and rice mycorrhizal roots. Promoter deletion assay revealed a 223-bp promoter fragment of SlHA8 containing a variant of AM-specific cis-element MYCS (vMYCS) sufficient to confer the AM-induced activity. Targeted deletion of this motif in the corresponding promoter region causes complete abolishment of GUS staining in mycorrhizal roots. Together, these results lend cogent evidence towards the evolutionary conservation of a potential regulatory mechanism mediating the activation of AM-responsive HA genes in diverse mycorrhizal plant species.
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Acknowledgments
This work was supported by the National Natural Science Foundation of China (31372121, 31572188), the Fundamental Research Funds for the Central Universities (KYTZ201404), A Foundation for the Author of National Excellent Doctoral Dissertation of PR China (FANEDD, 201264), and the Program for New Century Excellent Talents in University (NCET-12-0860). We thank Professor Yoram Kapulnik from the Volcani Center of Israel for kindly providing us the seeds of M161 mutant and Professor Hong Liao from the South China Agricultural University for providing the Agrobacterium rhizogenes strain K599. We also thank Dr. Ajay Jain from National Research Centre on Plant Biotechnology, Pusa campus, New Delhi, India, for valuable comments and carefully correcting the manuscript.
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Junli Liu and Jianjian Liu contributed equally to this work.
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Figure S1
Chromosomal organization of the tomato HA genes. (DOC 633 kb)
Figure S2
Multiple alignment of deduced amino acid sequences of tomato HA genes. (DOC 289 kb)
Figure S3
Expression analysis of NtHA8 and NtPT4 in leaves and roots of tobacco mycorrhizal and non-mycorrhizal plants. (DOC 108 kb)
Figure S4
Histochemical staining of the mycorrhizal or non-mycorrhizal roots harboring different deletions of SlHA8 promoter fragments driving the GUS reporter gene. (DOC 680 kb)
Table S1
Identity matrix for the eight SlHA genes and their predicted amino acid sequences. (DOC 38 kb)
Table S2
Chromosomal localizations and molecular features of tomato HA genes. (DOC 25 kb)
Table S3
Gene-specific primers used for Real-time RT-PCR amplification of tomato HA genes. (DOC 19 kb)
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Liu, J., Liu, J., Chen, A. et al. Analysis of tomato plasma membrane H+-ATPase gene family suggests a mycorrhiza-mediated regulatory mechanism conserved in diverse plant species. Mycorrhiza 26, 645–656 (2016). https://doi.org/10.1007/s00572-016-0700-9
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DOI: https://doi.org/10.1007/s00572-016-0700-9