RNase-Based Self-Incompatibility: Puzzled by<i>Pollen S</i>

Newbigin, Ed; Paape, Timothy; Kohn, Joshua R.

doi:10.1105/tpc.108.060327

Cited by 46 publications

(47 citation statements)

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“…The RNase activity of S-RNases is essential to the proper functioning of S-RNases in the selfincompatibility response (Huang et al, 1994), but it remains unclear just how the S-RNases can specifically affect the rejection of self-pollen. It has been reported recently that several S-locus F-box proteins control the functions of S-RNases through the ubiquitin/26S proteasome pathway of protein degradation (Qiao et al, 2004;Hua et al, 2007;Newbigin et al, 2008). These reports provide additional support to our hypothesis of the existence of a counterpart protein whose function is to control the regulatory roles of OmBBD in defense responses.…”

Section: Discussionsupporting

confidence: 80%

Novel Bifunctional Nucleases, OmBBD and AtBBD1, Are Involved in Abscisic Acid-Mediated Callose Deposition in Arabidopsis

You

Kim

et al. 2009

Plant Physiology

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Screening of the expressed sequence tag library of the wild rice species Oryza minuta revealed an unknown gene that was rapidly and strongly induced in response to attack by a rice fungal pathogen (Magnaporthe oryzae) and an insect (Nilaparvata lugens) and by wounding, abscisic acid (ABA), and methyl jasmonate treatments. Its recombinant protein was identified as a bifunctional nuclease with both RNase and DNase activities in vitro. This gene was designated OmBBD (for O. minuta bifunctional nuclease in basal defense response). Overexpression of OmBBD in an Arabidopsis (Arabidopsis thaliana) model system caused the constitutive expression of the PDF1.2, ABA1, and AtSAC1 genes, which are involved in priming ABA-mediated callose deposition. This activation of defense responses led to an increased resistance against Botrytis cinerea. atbbd1, the knockout mutant of the Arabidopsis ortholog AtBBD1, was susceptible to attack by B. cinerea and had deficient callose deposition. Overexpression of either OmBBD or AtBBD1 in atbbd1 plants complemented the susceptible phenotype of atbbd1 against B. cinerea as well as the deficiency of callose deposition. We suggest that OmBBD and AtBBD1 have a novel regulatory role in ABA-mediated callose deposition.

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Section: Discussionsupporting

confidence: 80%

Novel Bifunctional Nucleases, OmBBD and AtBBD1, Are Involved in Abscisic Acid-Mediated Callose Deposition in Arabidopsis

You

Kim

et al. 2009

Plant Physiology

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“…It is not obvious how SLFs and S-RNases came to constitute a genetic unit at a single S-locus during evolution of the S-RNase-based-SI system considering the much lower diversity among SLFs relative to S-RNases 11 . We conducted phylogenetic analysis of SLFs and S-RNases including those of other genera of Solanaceae by first exploring SLF-orthologs in the whole-genome databases of tomato (Solanum lycopersicum) and potato (Solanum tuberosum) 12,13 .…”

Section: Solanum S-loci Contain Orthologous Slf-like Paralogsmentioning

confidence: 99%

“…The model predicts that both S 17 -RNase and S 22 -RNase are the targets of conserved SLF1. We previously tested four conserved SLF1 alleles (S 5 , S 7 , S 9 , S 11 ) and showed that all of them targeted S 17 -RNase 9 . Our new experiment confirmed that S 22 -RNase is also the target of a conserved SLF1, S 7 -SLF1 ( Supplementary Fig.…”

Section: Diversity and Deletion Of Slfs Predict Target S-rnasementioning

confidence: 99%

“…We identified SLF genes from eight SI haplotypes (S 5 , S 7 , S 9 , S 10 , S 11 , S 17 , S 19 and S 22 ) and two self-compatible (SC) haplotypes (S m and S 0m ; see Online Methods) using a combination of next-generation sequencing (NGS) and PCR techniques. Initially, we constructed expressed sequence tag (EST) libraries from male reproductive organs of lines homozygous for each S-haplotype except S 10 , S 22 and S m , and then identified SLF-related sequences from these EST libraries.…”

Section: Petunia Pollen-s Consists Of Approximately 18 Slf Typesmentioning

confidence: 99%

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Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

et al. 2015

Self Cite

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Self-incompatibility (SI) systems in flowering plants distinguish self-and non-self pollen to prevent inbreeding. While other SI systems rely on the self-recognition between specific male-and femaledeterminants, the Solanaceae family has a non-self recognition system resulting in the detoxification of female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen. It is not known how many SLF components of this non-self recognition system there are in Solanaceae species, or how they evolved. We identified 16-20 SLFs in each S-haplotype in SI Petunia, from a total of 168 SLF sequences using large-scale nextgeneration sequencing and genomic polymerase chain reaction (PCR) techniques. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated these predictions by transformation experiments. A simple mathematical model confirmed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to the constitution of a non-self recognition system and also contribute to self-compatible mutations. Self-incompatibility (SI) systems in flowering plants distinguish self and non-self pollen to prevent inbreeding. While all other SI systems studied to date rely on the self-recognition between each single male-and female-determinants, the Solanaceae plants has a non-self recognition system that functions through the detoxification of non-self female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen.However, little is known about how many SLF components constitute such a non-self recognition system and how they evolve. Here we conducted large-scale next-generation sequencing and genomic PCR and identified 16-20 SLFs in each S-haplotype in SI Petunia, for a total of 168 SLF sequences. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated them by transformation experiments. A simple mathematical model showed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to constitute a non-self recognition system and as well as contributed to self-compatible mutations.SI is a genetically controlled reproductive barrier in angiosperms that allows the pistil to reject self (genetically-related) pollen and accept non-self (genetically-unrelated) pollen [1][2][3][4] . In most cases, this self/non-self discrimination is controlled by male-and

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“…The former is the S-ribonuclease gene (S-RNase) and the latter is a pollen-expressed F-box gene called the S haplotype-specific F-box gene (SFB) in Prunus of the Rosaceae and the S locus F-box gene (SLF) in the Solanaceae and Plantaginaceae (Entani et al, 2003;Lai et al, 2002;Qiao et al, 2004;Sijacic et al, 2004;Ushijima et al, 2003Ushijima et al, , 2004Yamane at al., 2003;Wang et al, 2004). Although the Prunus pollen S was originally referred to by two different terms, SFB and SLF (Entani et al, 2003), we use SFB in this article because it distinguishes the Prunus system from other systems, and recent studies have all used SFB (Newbigin et al, 2008;Sassa et al, 2010;Tao and Iezzoni, 2010). The S locus F-box brothers (SFBBs) have been identified as candidates for the pollen S determinant in the subtribe Pyrinae of the Rosaceae (De Franceschi et al, 2011a, 2011bKakui et al, 2011;Minamikawa et al, 2010;Okada et al, 2008Okada et al, , 2011Sassa et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Transcriptome Analysis of Self- and Cross-pollinated Pistils of Japanese Apricot (Prunus mume Sieb. et Zucc.)

Habu

Tao

2014

J. Japan. Soc. Hort. Sci.

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Solanaceae, Rosaceae, and Plantaginaceae exhibit the S-RNase-based gametophytic self-incompatibility (GSI) system. This type of GSI is controlled by a single polymorphic locus (S locus) containing the pistil S determinant gene, S-ribonuclease (S-RNase), and the pollen S determinant, the S locus F-box gene (SFB/SLF). In addition to these determinant genes, non-S factors, called modifier genes, are required for the GSI reaction. Here, we conducted large-scale transcriptome analysis of unpollinated, self-pollinated, and cross-pollinated pistils of Japanese apricot (Prunus mume Sieb. et Zucc. cv. Nanko) to capture all of the molecular events induced by the GSI reaction in Prunus, using next-generation sequencing technologies. We obtained 40,061 unigenes from 77,521,310 reads from pollinated and unpollinated pistils and pollen grains. Among these unigenes, 29,985 and 27,898 unigene sequences showed at least one hit against the NCBI nr and TAIR10 protein databases, respectively, in BLASTX searches using an E-value cutoff of 1e-6. Digital expression analysis showed that 8,907 and 10,190 unigenes were expressed at significantly different levels between unpollinated (UP) and cross-pollinated (CP) pistils and between UP and self-pollinated (SP) pistils, respectively. The expression of 4,348 unigenes in both CP and SP pollination was commonly and significantly different from that in UP, while the expression of 4,559 and 5,842 unigenes in CP and SP, respectively, was specifically and significantly different from UP. The expression of 2,227 unigenes was up-regulated both in CP and SP compared with UP. Genes supposedly involved in S-RNasebased GSI were included among the unigenes up-regulated by pollination, while no unigenes homologous to the solanaceous pistil modifiers HT-B or 120K were included among the unigenes up-regulated by pollination or in the whole unpollinated/pollinated pistil transcriptome. We discuss the distinct molecular mechanism of S-RNase-based GSI in Prunus.

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RNase-Based Self-Incompatibility: Puzzled byPollen S

Cited by 46 publications

References 50 publications

Novel Bifunctional Nucleases, OmBBD and AtBBD1, Are Involved in Abscisic Acid-Mediated Callose Deposition in Arabidopsis

Novel Bifunctional Nucleases, OmBBD and AtBBD1, Are Involved in Abscisic Acid-Mediated Callose Deposition in Arabidopsis

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

Transcriptome Analysis of Self- and Cross-pollinated Pistils of Japanese Apricot (Prunus mume Sieb. et Zucc.)

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