Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice ( Oryza sativa ). Received 14 January 2006. Accepted 17 April 2006. Available online 16 May 2006. Small auxin-up RNAs ( SAURs ) are the early auxin-responsive genes represented by a large multigene family in plants.
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Here, we report the identification of 58 OsSAUR gene family members from rice ( Oryza sativa japonica cv Nipponbare), the model monocot plant, by a reiterative database search and manual reannotation; 2 of these are pseudogenes. The coding sequences of OsSAURs do not possess any intron.
Most of the predicted OsSAUR protein sequences harbor a putative nuclear localization signal at their N-terminus. Localized gene duplications appear to be the primary genetic event responsible for SAUR gene family expansion in rice. Interestingly, the duplication of OsSAURs was found to be associated with the chromosomal block duplication as well. The phylogenetic analysis revealed that the SAUR gene family expanded in rice and Arabidopsis due to species-specific expansion of the family in monocots and dicots. The auxin-responsive elements and downstream element are conserved in the upstream and downstream sequences, respectively, of OsSAURs.
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In addition to the 21 OsSAURs with full-length cDNA sequences and 20 with expressed sequence tags, gene expression analyses of at least 7 OsSAURs by RT-qPCR indicated that the majority of identified OsSAURs most likely are expressed in rice. The transcript abundance of the OsSAURs examined increased within a few minutes of exogenous auxin application with varying kinetics. The present study provides basic genomic information for the rice SAUR gene family and will pave the way for deciphering the precise role of SAURs in plant growth and development. Auxin Evolution Expression Gene duplication Real-time PCR Rice ( Oryza sativa ) SAUR. The phytohormone auxin exerts a pleiotropic effect on various aspects of plant growth and development, including cell elongation, cell division, differentiation, root initiation, apical dominance, and tropic responses.
Auxin mediates these effects at the molecular level by altering the expression of numerous genes  and . The early auxin-responsive genes, which are specifically induced within minutes of auxin application, have been broadly grouped into three major classes: auxin/indoleacetic acid ( Aux/IAA ), GH3.
and small auxin-up RNA ( SAUR ) gene families . Apart from auxin, Aux / IAAs and SAUR s can be induced by cycloheximide, a translational inhibitor, indicating that their transcription is regulated by a short-lived repressor. There is increasing evidence that the Aux/IAA proteins act as repressors of gene transcription, regulating their own transcription . However, the function of SAURs largely remains obscure.
Following the initial identification of SAUR genes from soybean . members of this class have been isolated from mung bean . pea . Arabidopsis .
tobacco . and, more recently, maize  and . SAURs are represented as a large multigene family in the Arabidopsis genome comprising more than 70 members . The SAUR s encode highly unstable mRNAs with a very high turnover rate  and  that are induced within minutes by auxin application. The instability of SAUR mRNAs has been attributed due to the presence of a conserved downstream (DST) element in their 3′-untranslated regions  and . There is evidence that the SAURs are regulated at the posttranscriptional and posttranslational levels, too  and .
Recently, the calcium-dependent in vitro binding of SAUR proteins with calmodulin has been demonstrated  and . which provides a link between the Ca 2+ /calmodulin second messenger system and auxin signaling. The SAUR proteins remain largely uncharacterized.
Recently, the analysis of a nuclear-localized Zea mays SAUR protein, ZmSAUR2, has revealed that the SAUR proteins are short-lived, with a half-life of about 7 min . The SAUR transcripts are expressed mainly in the elongating tissues of soybean and maize .  and . indicating their role in auxin-mediated cell elongation. However, the exact role of SAURs in the auxin signaling hierarchy is still unknown. To understand the function and evolution of the SAUR s in plants, we analyzed the SAUR gene family in rice ( Oryza sativa ). Rice is one of the most important food crops and is considered the model monocot plant for molecular and genetic studies.
The complete rice genomic sequences are now available for two of the subspecies, indica  and japonica  and . Earlier, we identified and comprehensively analyzed the early auxin-responsive GH3 and Aux / IAA gene families from rice  and . Here, we report the genome-wide analysis of the rice SAUR ( OsSAUR ) gene family.
The work involved the identification of putative OsSAURs by reiterative database searches and manual reannotation. The phylogenetic analysis of SAURs from rice and Arabidopsis was performed to understand the possible mechanisms of gene family expansion. Also, the expression of OsSAURs has been analyzed using the full-length cDNAs and ESTs available in databases. The real-time PCR analysis of certain members demonstrated that OsSAURs are expressed in various rice organs/tissues and are induced very rapidly by exogenous auxin. Results and discussion.
Identification of the SAUR gene family in rice. The SAUR s are present as a multigene family in Arabidopsis comprising over 70 members . The availability of the complete rice genome sequence .  and  provided us the opportunity to find the OsSAURs in rice. The OsSAURs were identified in four steps from japonica subsp.
cv Nipponbare. The first step involved a BLASTP search of annotated proteins at The Institute for Genomic Research (TIGR) Rice Genome Annotation database using Arabidopsis SAUR protein sequences  as query. The second step aimed at a complete search for putative OsSAURs in rice and was performed by BLASTP and TBLASTN searches of the japonica cv Nipponbare genome sequences in GenBank at the National Center for Biotechnology Information (NCBI) utilizing Arabidopsis SAURs and all the rice SAUR proteins identified in the first step. All the OsSAURs identified were annotated as auxin-responsive/induced proteins at TIGR. However, many of the OsSAURs identified in the present study were annotated as unknown/hypothetical or expressed proteins and others as auxin-responsive/induced proteins at GenBank. In the third step, identical sequences present on the same or overlapping contigs in both the databases were identified and removed to obtain a set of nonredundant OsSAURs.
Each putative OsSAUR protein sequence was manually assessed for its sequence similarity to other putative OsSAURs or Arabidopsis thaliana (At) SAURs. Manual reannotation was performed to correct and reannotate the misannotated putative OsSAURs. Finally, as a last step, each predicted OsSAUR protein sequence was confirmed by a Pfam search for the presence of an auxin-inducible signature (PF02519) conserved in other SAUR proteins . The overall analysis revealed that the OsSAUR gene family comprises 58 members in rice, including 2 pseudogenes.
They were designated as OsSAUR1 to OsSAUR58 according to their position on the rice chromosomes, 1 to 12, and from top to bottom (Table 1. Fig. 1 A). The annotation of the two predicted pseudogenes seems to be correct as both of them are present on the completely sequenced bacterial artificial chromosomes (BACs); one of them ( OsSAUR43 ) showed the presence of a premature stop codon and the 5′ end was missing for the other ( OsSAUR50 ). Both the pseudogenes are present in the cluster of 17 OsSAURs on chromosome 9 and may have become nonfunctional after duplication. The predicted cDNA and protein sequences of all 58 OsSAURs are provided in Supplemental Data I and II.
Table 1. SAUR gene family in rice.