Independence and Interaction of Regions of the INNER NO OUTER Protein in Growth Control during Ovule Development

Gallagher, Thomas L.; Gasser, Charles S.

doi:10.1104/pp.107.114603

Cited by 19 publications

(17 citation statements)

References 20 publications

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“…However, our results indicate that despite clear orthology and conserved developmental roles, tomato and Arabidopsis INO proteins are not interchangeable as SlINO could not complement an Arabidopsis ino mutant when expressed from P- AtINO . This is in contrast to similar experiments with other paralogous Arabidopsis YABBY proteins, which promote varying levels of outer integument growth [ 38 , 41 ] despite lower levels of amino acid identity with AtINO (30 % to 35 %) than SlINO shares with AtINO (43 %). This result suggests that there are specific residues required for proper function of AtINO which are missing in SlINO, consistent with prior data that showed important determinants of AtINO function are distributed throughout the protein, rather than in a single structural domain [ 38 , 41 ].…”

Section: Discussioncontrasting

confidence: 99%

“…This is in contrast to similar experiments with other paralogous Arabidopsis YABBY proteins, which promote varying levels of outer integument growth [ 38 , 41 ] despite lower levels of amino acid identity with AtINO (30 % to 35 %) than SlINO shares with AtINO (43 %). This result suggests that there are specific residues required for proper function of AtINO which are missing in SlINO, consistent with prior data that showed important determinants of AtINO function are distributed throughout the protein, rather than in a single structural domain [ 38 , 41 ]. Taken together our results show that failure to complement in a heterologous expression experiment is not a reliable indicator that the proteins have diverged in their biological roles in the plants from which they derive.…”

Section: Discussioncontrasting

confidence: 99%

“…As a test of whether SlINO can function to support outer integument growth when expressed without regulatory constraints, a 35S:: SlINO transgene was introduced into Arabidopsis (L er ) segregating for the ino-1 mutation. At least 25 % of 42 transformants showed phenotypes commonly observed with ectopic overexpression of any active YABBY gene, such as curled leaves and carpels [ 38 ] (data not shown). The CaMV 35S promoter is not reliably expressed in ovules, but in 16 % of the 42 independent transformants (all among those showing the vegetative phenotypic effects) there was evidence that SlINO was acting to promote outer integument growth.…”

Section: Resultsmentioning

confidence: 99%

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Conservation of the role of INNER NO OUTER in development of unitegmic ovules of the Solanaceae despite a divergence in protein function

et al. 2016

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BackgroundThe INNER NO OUTER (INO) gene is expressed in the outermost cell layer of the outer integument of bitegmic ovules and is essential for this organ’s growth. The role and cross-species functional conservation of INO orthologs were examined in members of the Solanaceae, which have unitegmic ovules. Unitegmy has evolved several times in disparate angiosperm lineages. INO expression has been observed in the outermost cell layers of all examined unitegmic ovules, but the functional role of INO in unitegmic ovules has not previously been evaluated.ResultsINO orthologs were unambiguously identified in tobacco and tomato by sequence homology. Expression of the tomato INO gene was limited to the outer cell layer of the single integument indicating that this single integument has properties of the outer integument. Expression occurred only after integument initiation, later than observed in ovules of other examined angiosperms. Virus-induced knock-down of expression of the INO ortholog in tobacco inhibited growth of the outer cell layer of the integument leading to a decrease in both integument extension and curvature of the ovule. The altered ovules closely resemble those of the aberrant testa shape (ats) ino mutant combination in Arabidopsis where we see the effect of the ino mutation on a single fused integument produced by the ats mutation. Despite significant sequence identity and similar expression patterns, the tomato INO coding region was not able to complement the Arabidopsis ino mutant.ConclusionsThe similarity of effects of ino mutations on the unitegmic ovules of tobacco and the fused integuments of the Arabidopsis ats mutant show that: 1) INO orthologs play the same role in promoting integument growth in ovules of tobacco and Arabidopsis; and 2) the unitegmic ovules of tobacco (and hence other solanaceous species) are most likely the result of a congenital fusion of two ancestral integuments. Our results further indicate that INO has a conserved role in growth of the outermost cell layer of integuments. The curvature of solanaceous ovules is driven by unequal growth of the outer layers of the single integument that likely correspond to an ancestral outer integument.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-016-0835-z) contains supplementary material, which is available to authorized users.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussioncontrasting

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Conservation of the role of INNER NO OUTER in development of unitegmic ovules of the Solanaceae despite a divergence in protein function

et al. 2016

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“…Some of these interactors correspond to transcription or other regulatory factors potentially involved in different pathways. These include INNER NO OUTER (INO, At1g23420, involved in ovule outer integument development, [61] ), RESPONSE REGULATOR 14 (ARR14, At2g01760, involved in cytokinin signalling, [62] ), ABERRANT LATERAL ROOT FORMATION 14 (ALF4, At5g11030, involved in lateral root development, [63] ) from the Y2H-screen and PPD (involved in leaf development, [35] ), OBERON (OBE) and TITANIA (TTA) (both involved in embryonic root meristem initiation, [42] , [43] ), and SPINDLY (involved in cytokinin and gibberellin signalling, [45] , [64] ) reported here. The obe1 obe2 and tta1 tta2 double mutants are defective in root development [42] , [43] .…”

Section: Discussionmentioning

confidence: 99%

The Non-JAZ TIFY Protein TIFY8 from Arabidopsis thaliana Is a Transcriptional Repressor

et al. 2014

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Jasmonate (JA) signalling is mediated by the JASMONATE-ZIM DOMAIN (JAZ) repressor proteins, which are degraded upon JA perception to release downstream responses. The ZIM protein domain is characteristic of the larger TIFY protein family. It is currently unknown if the atypical member TIFY8 is involved in JA signalling. Here we show that the TIFY8 ZIM domain is functional and mediated interaction with PEAPOD proteins and NINJA. TIFY8 interacted with TOPLESS through NINJA and accordingly acted as a transcriptional repressor. TIFY8 expression was inversely correlated with JAZ expression during development and after infection with Pseudomonas syringae. Nevertheless, transgenic lines with altered TIFY8 expression did not show changes in JA sensitivity. Despite the functional ZIM domain, no interaction with JAZ proteins could be found. In contrast, TIFY8 was found in protein complexes involved in regulation of dephosphorylation, deubiquitination and O-linked N-acetylglucosamine modification suggesting an important role in nuclear signal transduction.

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“…In wus (wuschel) ovules both integuments are lacking and there is no normal curvature (Gross-Hardt et al, 2002). In ino (inner no outer), the outer integument is almost lacking (initiated but not further developed) but the inner is well developed, and there is no curvature (Baker et al, 1997;Schneitz et al, 1997;Villanueva et al, 1999;Gallagher and Gasser, 2008;Skinner and Gasser, 2009); the same was found in an ino mutant of the basal angiosperm Annona squamosa (Lora et al, 2011). In pfs2 ( pretty few seeds2) mutants with the PFS2 transgene some ovules are normal; however, in some ovules the outer integument is reduced (shorter than the inner) and the ovule is only halfway curved (Park et al, 2004(Park et al, , 2005.…”

Section: Development Of Curvature In Ovulesmentioning

confidence: 99%

Angiosperm ovules: diversity, development, evolution

2011

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In angiosperms the presence of an outer integument appears to be instrumental for ovule curvature, as indicated from studies on ovule diversity through the major clades of angiosperms, molecular developmental genetics in model species, abnormal ovules in a broad range of angiosperms, and comparison with gymnosperms with curved ovules. Lobation of integuments is not an atavism indicating evolution from telomes, but simply a morphogenetic constraint from the necessity of closure of the micropyle. Ovule shape is partly dependent on locule architecture, which is especially indicated by the occurrence of orthotropous ovules. Some ovule features are even more conservative than earlier assumed and thus of special interest in angiosperm macrosystematics.

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Independence and Interaction of Regions of the INNER NO OUTER Protein in Growth Control during Ovule Development

Cited by 19 publications

References 20 publications

Conservation of the role of INNER NO OUTER in development of unitegmic ovules of the Solanaceae despite a divergence in protein function

Conservation of the role of INNER NO OUTER in development of unitegmic ovules of the Solanaceae despite a divergence in protein function

The Non-JAZ TIFY Protein TIFY8 from Arabidopsis thaliana Is a Transcriptional Repressor

Angiosperm ovules: diversity, development, evolution

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