Dataset Information

Early Cold-Induced Peroxidases and Aquaporins Are Associated With High Cold Tolerance in Dajiao (Musa spp. 'Dajiao').

ABSTRACT: Banana is an important tropical fruit with high economic value. One of the main cultivars ('Cavendish') is susceptible to low temperatures, while another closely related specie ('Dajiao') has considerably higher cold tolerance. We previously reported that some membrane proteins appear to be involved in the cold tolerance of Dajiao bananas via an antioxidation mechanism. To investigate the early cold stress response of Dajiao, here we applied comparative membrane proteomics analysis for both cold-sensitive Cavendish and cold-tolerant Dajiao bananas subjected to cold stress at 10°C for 0, 3, and 6 h. A total of 2,333 and 1,834 proteins were identified in Cavendish and Dajiao, respectively. Subsequent bioinformatics analyses showed that 692 Cavendish proteins and 524 Dajiao proteins were predicted to be membrane proteins, of which 82 and 137 differentially abundant membrane proteins (DAMPs) were found in Cavendish and Dajiao, respectively. Interestingly, the number of DAMPs with increased abundance following 3 h of cold treatment in Dajiao (80) was seven times more than that in Cavendish (11). Gene ontology molecular function analysis of DAMPs for Cavendish and Dajiao indicated that they belong to eight categories including hydrolase activity, binding, transporter activity, antioxidant activity, etc., but the number in Dajiao is twice that in Cavendish. Strikingly, we found peroxidases (PODs) and aquaporins among the protein groups whose abundance was significantly increased after 3 h of cold treatment in Dajiao. Some of the PODs and aquaporins were verified by reverse-transcription PCR, multiple reaction monitoring, and green fluorescent protein-based subcellular localization analysis, demonstrating that the global membrane proteomics data are reliable. By combining the physiological and biochemical data, we found that membrane-bound Peroxidase 52 and Peroxidase P7, and aquaporins (MaPIP1;1, MaPIP1;2, MaPIP2;4, MaPIP2;6, MaTIP1;3) are mainly involved in decreased lipid peroxidation and maintaining leaf cell water potential, which appear to be the key cellular adaptations contributing to the cold tolerance of Dajiao. This membrane proteomics study provides new insights into cold stress tolerance mechanisms of banana, toward potential applications for ultimate genetic improvement of cold tolerance in banana.

SUBMITTER: He WD

PROVIDER: S-EPMC5852111 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Early Cold-Induced Peroxidases and Aquaporins Are Associated With High Cold Tolerance in Dajiao (<i>Musa</i> spp. 'Dajiao').

He Wei-Di WD Gao Jie J Dou Tong-Xin TX Shao Xiu-Hong XH Bi Fang-Cheng FC Sheng Ou O Deng Gui-Ming GM Li Chun-Yu CY Hu Chun-Hua CH Liu Ji-Hong JH Zhang Sheng S Yang Qiao-Song QS Yi Gan-Jun GJ

Frontiers in plant science 20180308

Banana is an important tropical fruit with high economic value. One of the main cultivars ('Cavendish') is susceptible to low temperatures, while another closely related specie ('Dajiao') has considerably higher cold tolerance. We previously reported that some membrane proteins appear to be involved in the cold tolerance of Dajiao bananas via an antioxidation mechanism. To investigate the early cold stress response of Dajiao, here we applied comparative membrane proteomics analysis for both cold ...[more]

PMID: 29568304

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Project description:BackgroundIn plants, RNA- based gene silencing mediated by small RNAs functions at the transcriptional or post-transcriptional level to negatively regulate target genes, repetitive sequences, viral RNAs and/or transposon elements. Post-transcriptional gene silencing (PTGS) or the RNA interference (RNAi) approach has been achieved in a wide range of plant species for inhibiting the expression of target genes by generating double-stranded RNA (dsRNA). However, to our knowledge, successful RNAi-application to knock-down endogenous genes has not been reported in the important staple food crop banana.ResultsUsing embryogenic cell suspension (ECS) transformed with ß-glucuronidase (GUS) as a model system, we assessed silencing of gusAINT using three intron-spliced hairpin RNA (ihpRNA) constructs containing gusAINT sequences of 299-nt, 26-nt and 19-nt, respectively. Their silencing potential was analysed in 2 different experimental set-ups. In the first, Agrobacterium-mediated co-transformation of banana ECS with a gusAINT containing vector and an ihpRNA construct resulted in a significantly reduced GUS enzyme activity 6-8 days after co-cultivation with either the 299-nt and 19-nt ihpRNA vectors. In the second approach, these ihpRNA constructs were transferred to stable GUS-expressing ECS and their silencing potential was evaluated in the regenerated in vitro plants. In comparison to control plants, transgenic plants transformed with the 299-nt gusAINT targeting sequence showed a 4.5 fold down-regulated gusA mRNA expression level, while GUS enzyme activity was reduced by 9 fold. Histochemical staining of plant tissues confirmed these findings. Northern blotting used to detect the expression of siRNA in the 299-nt ihpRNA vector transgenic in vitro plants revealed a negative relationship between siRNA expression and GUS enzyme activity. In contrast, no reduction in GUS activity or GUS mRNA expression occurred in the regenerated lines transformed with either of the two gusAINT oligo target sequences (26-nt and 19-nt).ConclusionsRNAi-induced silencing was achieved in banana, both at transient and stable level, resulting in significant reduction of gene expression and enzyme activity. The success of silencing was dependent on the targeted region of the target gene. The successful generation of transgenic ECS for second transformation with (an)other construct(s) can be of value for functional genomics research in banana.

Project description:Cold-sensitive Cavendish Banana and relatively cold-tolerant Dajiao (Musa spp.) comprise an important part of diets for millions of people around the globe. Low temperature is one of the key environment stresses which greatly affect the global banana production. However, little is known about the changes of global protein phosphorylation in Musa spp. and their regulatory roles in response to cold stress. In this study, we employed a TMT6-plex quantitative analysis to conduct a global phosphoproteome profiling between Cavendish Banana and Dajiao subject to the cold stress for 0 hour and 3 hour. A total of 679 phosphopeptides containing 772 distinct phosphorylated sites from 529 phosphoproteins were identified in Cavendish Banana, 180 phosphorylation sites (belonging to 147 phosphoproteins) were differentially changed after 3 h cold stress. While in Dajiao 241 phosphopeptides with 271 individual phosphosites from 207 phosphoproteins were confidently identified, and 83 phosphorylation sites from 63 phosphoproteins were differentially changed under 3 h cold stress. Bioinformatic analysis of protein interaction network indicated that Mitogen-activated protein kinase kinase 2 (MKK2) was located in the center of the MAPK signaling network along with 7 other members whose phosphorylated site abundances were remarkably differentiated between Cavendish Banana and Dajiao in response to cold stress. Western blotting of MKK2 protein and its T31 phosphorylated site showed the increased expression of MKK2 in the time course of cold stress, with no detectable T31 phosphorylation in Cavendish Banana. On the contrary, the decreased MKK2 expression with increased T31 phosphorylation was consistently observed in Dajiao. These results suggest that the MKK2 interaction network in Dajiao, along with other cold-specific phosphoproteins found in this study, appears to play an important role in the molecular mechanisms of Dajiao being high tolerance to cold stress. The results also provide new evidence that cellular MKK2 phosphorylation as a signaling pathway plays an important role in abiotic stress tolerance that serves as a universal plant cold tolerance mechanism. To the best of our knowledge, this is the first report of MKK2 network involved in the regulatory of the Musa spp. response to cold stress.

Dataset Information

Early Cold-Induced Peroxidases and Aquaporins Are Associated With High Cold Tolerance in Dajiao (Musa spp. 'Dajiao').

Publications

Early Cold-Induced Peroxidases and Aquaporins Are Associated With High Cold Tolerance in Dajiao (<i>Musa</i> spp. 'Dajiao').

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