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The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene.

Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H - J. Exp. Bot. (2010)

Bottom Line: MaMADS1, 2, and 3, are highly expressed in fruit only, while the others are expressed in fruit as well as in other organs.Only MaMADS2 is neither induced by ethylene nor by 1-MCP, and it is expressed mainly in pulp.Hence, our results are consistent with MaMADS2, a SEP3 homologue, acting in the pulp upstream of the increase in ethylene production similarly to LeMADS-RIN.

View Article: PubMed Central - PubMed

Affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization (ARO), the Volcani Center, PO Box 6, Bet Dagan 50250, Israel.

ABSTRACT
Six MaMADS-box genes have been cloned from the banana fruit cultivar Grand Nain. The similarity of these genes to tomato LeRIN is low and neither MaMADS2 nor MaMADS1 complement the tomato rin mutation. Nevertheless, the expression patterns, specifically in fruit and the induction during ripening and in response to ethylene and 1-MCP, suggest that some of these genes may participate in ripening. MaMADS1, 2, and 3, are highly expressed in fruit only, while the others are expressed in fruit as well as in other organs. Moreover, the suites of MaMADS-box genes and their temporal expression differ in peel and pulp during ripening. In the pulp, the increase in MaMADS2, 3, 4, and 5 expression preceded an increase in ethylene production, but coincides with the CO(2) peak. However, MaMADS1 expression in pulp coincided with ethylene production, but a massive increase in its expression occurred late during ripening, together with a second wave in the expression of MaMADS2, 3, and 4. In the peel, on the other hand, an increase in expression of MaMADS1, 3, and to a lesser degree also of MaMADS4 and 2 coincided with an increase in ethylene production. Except MaMADS3, which was induced by ethylene in pulp and peel, only MaMADS4, and 5 in pulp and MaMADS1 in peel were induced by ethylene. 1-MCP applied at the onset of the increase in ethylene production, increased the levels of MaMADS4 and MaMADS1 in pulp, while it decreased MaMADS1, 3, 4, and 5 in peel, suggesting that MaMADS4 and MaMADS1 are negatively controlled by ethylene at the onset of ethylene production only in pulp. Only MaMADS2 is neither induced by ethylene nor by 1-MCP, and it is expressed mainly in pulp. Our results suggest that two independent ripening programs are employed in pulp and peel which involve the activation of mainly MaMADS2, 4, and 5 and later on also MaMADS1 in pulp, and mainly MaMADS1, and 3 in peel. Hence, our results are consistent with MaMADS2, a SEP3 homologue, acting in the pulp upstream of the increase in ethylene production similarly to LeMADS-RIN.

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Isolation of MaMADS-box genes from Cavendish banana (cultivar Grand Nain). (A) Putative proteins alignment of MaMADS1–6 sequences isolated from banana fruit and the similarity among them. The gene sequences were deposited in http://www.ncbi.nlm.nih.gov/BLAST as EU869307, EU869306, EU869308, EU869309, EU869310, and EU869311, respectively. (B) Phylogenetic analysis of MaMADS1–4 with other SEP3 clade genes. The analysis was performed on the full-lengths of the individual genes. The SEP3 motif for each of the genes is presented on the right. The genes included in this alignment are: AoAOM1 (AAQ83834), SISEP3 (BAD10945.1), LItuAGL9 (AAX15920.1), PaAGL9.1 (AAX15923.1), HcSEP1 (BAC80253.1), PsM6 (AAX69068), DcSEP1 (AAZ95252.1), AdMADS (CAA48859.1), SaMADSD (CAA69916.1), PsMADS (CAA11258.1), PhFBP26 (AAF19164.1), NsMADS3 (AAD39034.1), LeTM5 (AAP57413.1), EcAGL9 (AAX15918.1), DeCDM44 (AAO22982.1), BpMADS (CAB95648.1), DEFH200 (CAA64743.1), PtMADS6 (AAO49811.1), AtSEP (AAT46095.1), VvMADS4 (AAM21344.1), AmDEFH72 (CAA64742.1). (C) Phylogenetic analysis of MaMADS5 with other AG genes. The existence of AG motifs for all the genes is shown. The genes included in this alignment are: DtSEEDSTICK (AAY86365.1), DnMADS2 (ABQ08574.1), AvMADS (BAD83772.1), HoMADS1 (AAF08830.2). (D) Phylogenetic analysis of MaMADS6 with other PI genes. The existence of PI motifs for all the genes are shown. The genes included in this alignment are: AoPI (ABB92623.1), P9PI (AAV28175.1), PI10 (AAV28490.1), HPI2 (AAD22494.2), PI1 (ABG90945.1). Lines underneath the genes mark the genes isolated from banana. Stars and dots indicate identity and similarity, respectively.
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fig1: Isolation of MaMADS-box genes from Cavendish banana (cultivar Grand Nain). (A) Putative proteins alignment of MaMADS1–6 sequences isolated from banana fruit and the similarity among them. The gene sequences were deposited in http://www.ncbi.nlm.nih.gov/BLAST as EU869307, EU869306, EU869308, EU869309, EU869310, and EU869311, respectively. (B) Phylogenetic analysis of MaMADS1–4 with other SEP3 clade genes. The analysis was performed on the full-lengths of the individual genes. The SEP3 motif for each of the genes is presented on the right. The genes included in this alignment are: AoAOM1 (AAQ83834), SISEP3 (BAD10945.1), LItuAGL9 (AAX15920.1), PaAGL9.1 (AAX15923.1), HcSEP1 (BAC80253.1), PsM6 (AAX69068), DcSEP1 (AAZ95252.1), AdMADS (CAA48859.1), SaMADSD (CAA69916.1), PsMADS (CAA11258.1), PhFBP26 (AAF19164.1), NsMADS3 (AAD39034.1), LeTM5 (AAP57413.1), EcAGL9 (AAX15918.1), DeCDM44 (AAO22982.1), BpMADS (CAB95648.1), DEFH200 (CAA64743.1), PtMADS6 (AAO49811.1), AtSEP (AAT46095.1), VvMADS4 (AAM21344.1), AmDEFH72 (CAA64742.1). (C) Phylogenetic analysis of MaMADS5 with other AG genes. The existence of AG motifs for all the genes is shown. The genes included in this alignment are: DtSEEDSTICK (AAY86365.1), DnMADS2 (ABQ08574.1), AvMADS (BAD83772.1), HoMADS1 (AAF08830.2). (D) Phylogenetic analysis of MaMADS6 with other PI genes. The existence of PI motifs for all the genes are shown. The genes included in this alignment are: AoPI (ABB92623.1), P9PI (AAV28175.1), PI10 (AAV28490.1), HPI2 (AAD22494.2), PI1 (ABG90945.1). Lines underneath the genes mark the genes isolated from banana. Stars and dots indicate identity and similarity, respectively.

Mentions: Six full-length transcripts were cloned from the banana fruit of the cultivar Grand Nain of the Cavendish subgroup (Fig. 1). Each one of them exhibited a difference in the amino acid (aa) sequence, when compared to the homologuos partial sequences from other other banana cultivars deposited in GenBank, (data not shown). Alignment of the putative aa of the six genes showed high similarity in the two regions: 1 to about 55 aa–M domain, and around 95 to about 170 aa–K domain (Fig. 1A). The genes were highly variable in their C domain. Phylogenetic analysis of these genes with MADS-box genes from various clades revealed that the genes MaMADS1–4 belong the SEP3 clade and indeed they contain the SEP3 motif (Fig. 1B) (Malcomber and Kellogg, 2005). The genes MaMADS2 and 4 show the highest similarity between them and the highest to LeMADS-RIN (Table 1). The genes MaMADS5 and MaMADS6 belong to the AGAMOUS (AG) and PISTILLATA (PI) clades, respectively. These genes indeed contain the respective domains (Fig. 1 C, D) (Skipper et al., 2006). Comparing the C-terminus of all the banana genes to that of LeMADS-RIN from tomato showed lower homology to Le-MADS-RIN than when the whole gene is compared (Table 1). (Similarities are: 30% for MaMADS1, 35% for MaMADS2, 28% for MaMADS3, 32% for MaMADS4, 20% for MaMADS5, and 15% for the gene MaMADS6). The genes isolated have shown the highest homology to the corresponding genes: MaMADS1: 75% similarity to AOM1 (AAQ83834 from Asparagus officinalis) (Caporali et al., 2000), MaMADS2 and MaMADS4: 88% and 84% similarity, respectively, to MADS-box (AAQ03226 from Elaeis guineensis) (Adam et al., 2006), MaMADS3: 78% similarity to AGL9a (ABK35281from Crocus sativus). MaMADS5: 85% similarity to MADS (BAD83772 from Asparagus virgatus), MaMADS6: 88% similarity to PISTILLATA-like protein (ABB92623 Alpinia oblongifolia) (Gao et al., 2006).


The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene.

Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H - J. Exp. Bot. (2010)

Isolation of MaMADS-box genes from Cavendish banana (cultivar Grand Nain). (A) Putative proteins alignment of MaMADS1–6 sequences isolated from banana fruit and the similarity among them. The gene sequences were deposited in http://www.ncbi.nlm.nih.gov/BLAST as EU869307, EU869306, EU869308, EU869309, EU869310, and EU869311, respectively. (B) Phylogenetic analysis of MaMADS1–4 with other SEP3 clade genes. The analysis was performed on the full-lengths of the individual genes. The SEP3 motif for each of the genes is presented on the right. The genes included in this alignment are: AoAOM1 (AAQ83834), SISEP3 (BAD10945.1), LItuAGL9 (AAX15920.1), PaAGL9.1 (AAX15923.1), HcSEP1 (BAC80253.1), PsM6 (AAX69068), DcSEP1 (AAZ95252.1), AdMADS (CAA48859.1), SaMADSD (CAA69916.1), PsMADS (CAA11258.1), PhFBP26 (AAF19164.1), NsMADS3 (AAD39034.1), LeTM5 (AAP57413.1), EcAGL9 (AAX15918.1), DeCDM44 (AAO22982.1), BpMADS (CAB95648.1), DEFH200 (CAA64743.1), PtMADS6 (AAO49811.1), AtSEP (AAT46095.1), VvMADS4 (AAM21344.1), AmDEFH72 (CAA64742.1). (C) Phylogenetic analysis of MaMADS5 with other AG genes. The existence of AG motifs for all the genes is shown. The genes included in this alignment are: DtSEEDSTICK (AAY86365.1), DnMADS2 (ABQ08574.1), AvMADS (BAD83772.1), HoMADS1 (AAF08830.2). (D) Phylogenetic analysis of MaMADS6 with other PI genes. The existence of PI motifs for all the genes are shown. The genes included in this alignment are: AoPI (ABB92623.1), P9PI (AAV28175.1), PI10 (AAV28490.1), HPI2 (AAD22494.2), PI1 (ABG90945.1). Lines underneath the genes mark the genes isolated from banana. Stars and dots indicate identity and similarity, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2837265&req=5

fig1: Isolation of MaMADS-box genes from Cavendish banana (cultivar Grand Nain). (A) Putative proteins alignment of MaMADS1–6 sequences isolated from banana fruit and the similarity among them. The gene sequences were deposited in http://www.ncbi.nlm.nih.gov/BLAST as EU869307, EU869306, EU869308, EU869309, EU869310, and EU869311, respectively. (B) Phylogenetic analysis of MaMADS1–4 with other SEP3 clade genes. The analysis was performed on the full-lengths of the individual genes. The SEP3 motif for each of the genes is presented on the right. The genes included in this alignment are: AoAOM1 (AAQ83834), SISEP3 (BAD10945.1), LItuAGL9 (AAX15920.1), PaAGL9.1 (AAX15923.1), HcSEP1 (BAC80253.1), PsM6 (AAX69068), DcSEP1 (AAZ95252.1), AdMADS (CAA48859.1), SaMADSD (CAA69916.1), PsMADS (CAA11258.1), PhFBP26 (AAF19164.1), NsMADS3 (AAD39034.1), LeTM5 (AAP57413.1), EcAGL9 (AAX15918.1), DeCDM44 (AAO22982.1), BpMADS (CAB95648.1), DEFH200 (CAA64743.1), PtMADS6 (AAO49811.1), AtSEP (AAT46095.1), VvMADS4 (AAM21344.1), AmDEFH72 (CAA64742.1). (C) Phylogenetic analysis of MaMADS5 with other AG genes. The existence of AG motifs for all the genes is shown. The genes included in this alignment are: DtSEEDSTICK (AAY86365.1), DnMADS2 (ABQ08574.1), AvMADS (BAD83772.1), HoMADS1 (AAF08830.2). (D) Phylogenetic analysis of MaMADS6 with other PI genes. The existence of PI motifs for all the genes are shown. The genes included in this alignment are: AoPI (ABB92623.1), P9PI (AAV28175.1), PI10 (AAV28490.1), HPI2 (AAD22494.2), PI1 (ABG90945.1). Lines underneath the genes mark the genes isolated from banana. Stars and dots indicate identity and similarity, respectively.
Mentions: Six full-length transcripts were cloned from the banana fruit of the cultivar Grand Nain of the Cavendish subgroup (Fig. 1). Each one of them exhibited a difference in the amino acid (aa) sequence, when compared to the homologuos partial sequences from other other banana cultivars deposited in GenBank, (data not shown). Alignment of the putative aa of the six genes showed high similarity in the two regions: 1 to about 55 aa–M domain, and around 95 to about 170 aa–K domain (Fig. 1A). The genes were highly variable in their C domain. Phylogenetic analysis of these genes with MADS-box genes from various clades revealed that the genes MaMADS1–4 belong the SEP3 clade and indeed they contain the SEP3 motif (Fig. 1B) (Malcomber and Kellogg, 2005). The genes MaMADS2 and 4 show the highest similarity between them and the highest to LeMADS-RIN (Table 1). The genes MaMADS5 and MaMADS6 belong to the AGAMOUS (AG) and PISTILLATA (PI) clades, respectively. These genes indeed contain the respective domains (Fig. 1 C, D) (Skipper et al., 2006). Comparing the C-terminus of all the banana genes to that of LeMADS-RIN from tomato showed lower homology to Le-MADS-RIN than when the whole gene is compared (Table 1). (Similarities are: 30% for MaMADS1, 35% for MaMADS2, 28% for MaMADS3, 32% for MaMADS4, 20% for MaMADS5, and 15% for the gene MaMADS6). The genes isolated have shown the highest homology to the corresponding genes: MaMADS1: 75% similarity to AOM1 (AAQ83834 from Asparagus officinalis) (Caporali et al., 2000), MaMADS2 and MaMADS4: 88% and 84% similarity, respectively, to MADS-box (AAQ03226 from Elaeis guineensis) (Adam et al., 2006), MaMADS3: 78% similarity to AGL9a (ABK35281from Crocus sativus). MaMADS5: 85% similarity to MADS (BAD83772 from Asparagus virgatus), MaMADS6: 88% similarity to PISTILLATA-like protein (ABB92623 Alpinia oblongifolia) (Gao et al., 2006).

Bottom Line: MaMADS1, 2, and 3, are highly expressed in fruit only, while the others are expressed in fruit as well as in other organs.Only MaMADS2 is neither induced by ethylene nor by 1-MCP, and it is expressed mainly in pulp.Hence, our results are consistent with MaMADS2, a SEP3 homologue, acting in the pulp upstream of the increase in ethylene production similarly to LeMADS-RIN.

View Article: PubMed Central - PubMed

Affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization (ARO), the Volcani Center, PO Box 6, Bet Dagan 50250, Israel.

ABSTRACT
Six MaMADS-box genes have been cloned from the banana fruit cultivar Grand Nain. The similarity of these genes to tomato LeRIN is low and neither MaMADS2 nor MaMADS1 complement the tomato rin mutation. Nevertheless, the expression patterns, specifically in fruit and the induction during ripening and in response to ethylene and 1-MCP, suggest that some of these genes may participate in ripening. MaMADS1, 2, and 3, are highly expressed in fruit only, while the others are expressed in fruit as well as in other organs. Moreover, the suites of MaMADS-box genes and their temporal expression differ in peel and pulp during ripening. In the pulp, the increase in MaMADS2, 3, 4, and 5 expression preceded an increase in ethylene production, but coincides with the CO(2) peak. However, MaMADS1 expression in pulp coincided with ethylene production, but a massive increase in its expression occurred late during ripening, together with a second wave in the expression of MaMADS2, 3, and 4. In the peel, on the other hand, an increase in expression of MaMADS1, 3, and to a lesser degree also of MaMADS4 and 2 coincided with an increase in ethylene production. Except MaMADS3, which was induced by ethylene in pulp and peel, only MaMADS4, and 5 in pulp and MaMADS1 in peel were induced by ethylene. 1-MCP applied at the onset of the increase in ethylene production, increased the levels of MaMADS4 and MaMADS1 in pulp, while it decreased MaMADS1, 3, 4, and 5 in peel, suggesting that MaMADS4 and MaMADS1 are negatively controlled by ethylene at the onset of ethylene production only in pulp. Only MaMADS2 is neither induced by ethylene nor by 1-MCP, and it is expressed mainly in pulp. Our results suggest that two independent ripening programs are employed in pulp and peel which involve the activation of mainly MaMADS2, 4, and 5 and later on also MaMADS1 in pulp, and mainly MaMADS1, and 3 in peel. Hence, our results are consistent with MaMADS2, a SEP3 homologue, acting in the pulp upstream of the increase in ethylene production similarly to LeMADS-RIN.

Show MeSH
Related in: MedlinePlus