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Genome-wide analysis of Aux/IAA gene family in Solanaceae species using tomato as a model

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Abstract

Auxin plays key roles in a wide variety of plant activities, including embryo development, leaf formation, phototropism, fruit development and root initiation and development. Auxin/indoleacetic acid (Aux/IAA) genes, encoding short-lived nuclear proteins, are key regulators in the auxin transduction pathway. But how they work is still unknown. In order to conduct a systematic analysis of this gene family in Solanaceae species, a genome-wide search for the homologues of auxin response genes was carried out. Here, 26 and 27 non redundant AUX/IAAs were identified in tomato and potato, respectively. Using tomato as a model, a comprehensive overview of SlIAA gene family is presented, including the gene structures, phylogeny, chromosome locations, conserved motifs and cis-elements in promoter sequences. A phylogenetic tree generated from alignments of the predicted protein sequences of 31 OsIAAs, 29 AtIAAs, 31 ZmIAAs, and 26 SlIAAs revealed that these IAAs were clustered into three major groups and ten subgroups. Among them, seven subgroups were present in both monocot and dicot species, which indicated that the major functional diversification within the IAA family predated the monocot/dicot divergence. In contrast, group C and some other subgroups seemed to be species-specific. Quantitative real-time PCR (qRT-PCR) analysis showed that 19 of the 26 SlIAA genes could be detected in all tomato organs/tissues, however, seven of them were specifically expressed in some of tomato tissues. The transcript abundance of 17 SlIAA genes were increased within a few hours when the seedlings were treated with exogenous IAA. However, those of other six SlIAAs were decreased. The results of stress treatments showed that most SIIAA family genes responded to at least one of the three stress treatments, however, they exhibited diverse expression levels under different abiotic stress conditions in tomato seedlings. SlIAA20, SlIAA21 and SlIAA22 were not significantly influenced by stress treatments even though at least one stress-related cis-element was identified in their promoter regions. In conclusion, our comparative analysis provides an insight into the evolution and expression patterns in various tissues and in response to auxin or stresses of the Aux/IAA family members in tomato, which will provide a very useful reference for cloning and functional analysis of each member of AUX/IAA gene family in Solanaceae crops.

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Abbreviations

ARF:

Auxin response factor

Aux/IAA:

Auxin/indoleacetic acid

AuxRE:

Auxin responsive elements

NLS:

Nuclear localization signal

qRT-PCR:

Quantitative real-time PCR

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Acknowledgments

This work was supported by the State Key Basic Research and Development Plan of China (2009CB119000), the National Natural Science Foundation of China (30771470) and Zhejiang Provincial Natural Science Foundation of China (R3110209 and 2009C32025). Sequence data from this article can be found in the GenBank/EMBL data libraries under the following accession numbers: JN043331(SlIAA12), JN043332(SlIAA13), JN043333(SlIAA16).

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Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Growth, Development and Biotechnology, Agricultural Ministry of China, Department of Horticulture, Zhejiang University, 310058, Hangzhou, People’s Republic of China

    Jian Wu, Zhen Peng, Songyu Liu, Yanjun He, Lin Cheng, Fuling Kong, Jie Wang & Gang Lu

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  1. Jian Wu
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  2. Zhen Peng
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  3. Songyu Liu
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Corresponding author

Correspondence to Gang Lu.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Table S1. PCR Primer sequences for SlIAAs isolation. (DOC 29 kb)

Table S2 Primer sequences for qRT-PCR expression analysis. (DOC 56 kb)

Table S3 IAA genes in tobacco. (DOC 43 kb)

Table S4.Cis-elements in the promoters of SlIAA genes. (DOC 85 kb)

Table S5. Expression features of tomato Aux/IAA genes in responsive to various treatments (DOC 40 kb)

438_2012_675_MOESM6_ESM.xls

Table S6. The expression analysis of AtIAA family genes in various Arabidopsis tissues. The expression data were searched against Arabidopsis eFP Browser using the AtIAA gene accession number (XLS 31 kb)

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Table S7. The expression analysis of AtIAA family genes in response to auxin and abiotic treatments. The expression data were serached against Arabidopsis eFP Browser using each AtIAA gene accession number. (XLS 23 kb)

Supplemental Figure 8. Promoter regions of 26 SlIAAs. (DOC 76 kb)

Supplemental Figure 9. Amino acid sequences of 26 SlIAAs. (DOC 30 kb)

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Supplemental Figure 10. Alignment of potato Aux/IAA proteins obtained with the ClustalX program. The height of the bars indicates the number of identical residues per position. b: Multiple alignments of the domains I to IV of the tomato Aux/IAA proteins obtained with ClustalX and manual correction. Black and light gray shading indicate identical and conversed amino acid residues, respectively. Conserved domains are also underlined and correspond to part a. (JPEG 1417 kb)

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Supplemental Figure 11 a. Alignment of tobacco Aux/IAA proteins obtained with the ClustalX program. The height of the bars indicates the number of identical residues per position. b: Multiple alignments of the domains I to IV of the tobacco Aux/IAA proteins obtained with ClustalX and manual correction. Black and light gray shading indicate identical and conversed amino acid residues, respectively. Conserved domains are also underlined and correspond to part a. (JPEG 936 kb)

438_2012_675_MOESM12_ESM.jpg

Supplemental Figure 12. The five conserved consensus motifs in AUX/IAA of tomato, rice, maize and Arabidopsis IAA proteins were found by MEME. The symbol heights represent the relative frequency of each residue. The numbers of sites and e-value for each motif are also shown. (JPEG 432 kb)

Supplemental Figure 13. Auxin signaling transduction related cis-element in the promoters of SlIAA genes. (JPEG 413 kb)

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Supplemental Figure 14. Expression profiles of all the 26 SlIAA genes in different tomato flower tissues. qRT-PCR analyses using RNA generated from sepal (Se), petal (P), stamen (St), and ovary (O) were performed. For other details see Figure 5. (JPEG 557 kb)

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Supplemental Figure 15. Expression profiles of all the 26 SlIAA genes at different tomato flower developmental stages. QRT-PCR analyses were performed using RNA generated from tomato flower buds at three stages of early floral development, roughly defined by the length of flower buds as follows: stage I: 3-4 mm, stage II: 5-6 mm, and stage III at 7-8 mm. (JPEG 485 kb)

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Supplemental Figure 16. Expression profiles of all the 26 SlIAA genes in response to environmental stress. QRT-PCR analyses were used to assess SlIAA transcript levels in tomato seedlings exposed to drought (D), salt (S), heat (H) stresses when compared to control treatment. (JPEG 604 kb)

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Supplemental Figure 17. Phylogenetic relationships among the potato, tomato and tobacco IAA proteins. The unrooted tree was generated using MEGA4.1 program by the neighbor-joining method. Bootstrap support from 1000 replicates are indicated at each branch. (JPEG 90 kb)

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Supplemental Figure 18. Phylogenetic relationships among the Arabidopsis IAA proteins. The unrooted tree was generated using MEGA4.1 program by the neighbor-joining method. Bootstrap support from 1000 replicates are indicated at each branch. (JPEG 37 kb)

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Supplemental Figure 19. Phylogenetic relationships among the maize IAA proteins. The unrooted tree was generated using MEGA4.1 program by the neighbor-joining method. Bootstrap support from 1000 replicates are indicated at each branch. (JPEG 34 kb)

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Supplemental Figure 20. Phylogenetic relationships among the rice IAA proteins. The unrooted tree was generated using MEGA4.1 program by the neighbor-joining method. Bootstrap supports from 1000 replicates are indicated at each branch. (JPEG 38 kb)

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Wu, J., Peng, Z., Liu, S. et al. Genome-wide analysis of Aux/IAA gene family in Solanaceae species using tomato as a model. Mol Genet Genomics 287, 295–311 (2012). https://doi.org/10.1007/s00438-012-0675-y

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