Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress - PubMed (original) (raw)

Comparative Study

Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress

Qiao-Song Yang et al. BMC Genomics. 2015.

Abstract

Background: Banana and plantain (Musa spp.) comprise an important part of diets for millions of people around the globe. Low temperature is one of the key environmental stresses which greatly affects the global banana production. To understand the molecular mechanism of the cold-tolerance in plantain we used RNA-Seq based comparative transcriptomics analyses for both cold-sensitive banana and cold-tolerant plantain subjected to the cold stress for 0, 3 and 6 h.

Results: The cold-response genes at early stage are identified and grouped in both species by GO analysis. The results show that 10 and 68 differentially expressed genes (DEGs) are identified for 3 and 6 h of cold stress respectively in plantain, while 40 and 238 DEGs are identified respectively in banana. GO classification analyses show that the majority of DEGs identified in both banana and plantain belong to 11 categories including regulation of transcription, response to stress signal transduction, etc. A similar profile for 28 DEGs was found in both banana and plantain for 6 h of cold stress, suggesting both share some common adaptation processes in response to cold stress. There are 17 DEGs found uniquely in cold-tolerance plantain, which were involved in signal transduction, abiotic stress, copper ion equilibrium, photosynthesis and photorespiration, sugar stimulation, protein modifications etc. Twelve early responsive genes including ICE1 and MYBS3 were selected and further assessed and confirmed by qPCR in the extended time course experiments (0, 3, 6, 24 and 48 h), which revealed significant expression difference of key genes in response to cold stress, especially ICE1 and MYBS3 between cold-sensitive banana and cold-tolerant plantain.

Conclusions: We found that the cold-tolerance pathway appears selectively activated by regulation of ICE1 and MYBS3 expression in plantain under different stages of cold stress. We conclude that the rapid activation and selective induction of ICE1 and MYBS3 cold tolerance pathways in plantain, along with expression of other cold-specific genes, may be one of the main reasons that plantain has higher cold resistance than banana.

PubMed Disclaimer

Figures

Figure 1

Figure 1

Phenotypic and physiological responses of banana and plantain under cold stress. Six-leaf stage seedlings of banana and plantain were treated at 10°C for 0, 3 and 6 h (A); and comparison of phenotypic difference of the three leaves from the top of banana and plantain following 48 h of cold treatment (B); the relative electrolyte leakage was determined for the banana and plantain treated at 10°C for 0, 3, 6, 24 and 48 h. The different letters (lowercase letters-banana, capital letters-plantain) labeled above columns indicate a significant difference at p ≤ 0.05 between the columns by Duncan’s test using SPSS statistical software (version 16.0, SPSS Inc. Chicago, IL). The columns with the same letters mean no significant difference (p > 0.05) between each other (C).

Figure 2

Figure 2

Venn diagram of differentially expressed genes (DEGs) identified for cold-sensitive banana and cold-tolerant plantain in response to cold stress. Green circle segment: the number of DEGs in banana under cold treatment at 10°C for 3 h with 0 h of banana as a control; Purple circle segment: the number of DEGs in banana under cold treatment at 10°C for 6 h, 0 h of banana as a control; Red circle segment: the number of DEGs in plantain under cold treatment at 10°C for 3 h, 0 h of plantain as a control; Black circle segment: the number of DEGs in plantain under cold treatment at 10°C for 6 h, 0 h of plantain as a control.

Figure 3

Figure 3

Relative mRNA levels of 12 DEGs in banana and plantain seedlings were determined by quantitative RT-PCR analyses. Six-leaf stage seedlings were incubated at 10°C for the indicated time. Transcript abundances of genes encoding dehydration-responsive element-binding protein 1D (A), ethylene insensitive 3-like 1 protein (B), probable cytosolic iron-sulfur protein assembly protein 1 (C), zinc finger protein 1 (D), U-box domain- containing protein 25 (E), zinc finger CCCH domain-containing protein 33 (F), UDP-glucose 6-dehydrogenase (G), probable xyloglucan endotransglucosylase/hydrolase protein 23 (H), ethylene-responsive transcription factor RAP2-13 (I), calcium-binding protein KIC (J), transcription factor ICE1 (K) and MYBS3 (L) from both banana and plantain were determined and compared across the time course of cold stress. Data represent means ± SD in four replicates (n = 4). The different lowercase letters labeled above columns indicate a significant difference at p ≤ 0.05 between the columns by Duncan’s test using SPSS statistical software (version 16.0, SPSS Inc. Chicago, IL). The columns with the same letters mean no significant difference (p > 0.05) between each other.

Figure 4

Figure 4

A schematic diagram of cold-tolerance transcriptional network in plantain, adapted initially from V. Chinnusamy et al. (2007) [4] and C.F. Su et al. (2010) [14] and revised based on this study. At the early stage of cold stress, plantain cells probably sense low temperatures through membrane rigidification and/or other cellular changes, which might induce a calcium signature and activate protein kinases necessary for cold tolerance. Constitutively expressed ICE1 is activated by cold stress through sumoylation and phosphorylation. Sumoylation of ICE1 is critical for ICE1-activation of transcription of CBFs and repression of MYB15. CBFs regulate the expression of COR genes that confer cold tolerance. The expression of CBFs is negatively regulated by MYB15. HOS1 mediates the ubiquitination and proteosomal degradation of ICE1 and, thus, negatively regulates CBF regulons. CBFs can constitutively regulate the expression of downstream cold-responsive transcription factor genes RAPs, which might control sub-regulons of the CBF regulon. CBFs also activate αAmy3 expression to hydrolyse reserved starch. At the late stage of cold stress,MYBS3 inhibits CBFs and αAmy3 expression. The effective coordination across the early and late stages of cold stress by at least two different regulatory pathways appears to efficiently regulate the following metabolic pathways including oxidation reduction, oxylipin biosynthetic process, photosynthesis, photorespiration, glycolysis, tricarboxylic acid cycle, carbohydrate metabolic process, fatty acid biosynthetic process and beta-oxidation. The rapid activation and selective induction of ICE1 and MYBS3 cold tolerance pathways in plantain, along with expression of other cold-specific genes, may be one of the main reasons that plantain has higher cold resistance than banana (Heatmaps show the expression of ICE1 and MYBS3 in banana and plantain under cold stress). Broken arrows indicate post-translational regulation; solid arrows indicate activation, whereas lines ending with a bar show negative regulation; the two stars (**) indicate unknown cis-elements. P, phosphorylation; S, SUMO; U, ubiquitin.

Similar articles

Cited by

References

    1. Zhou MQ, Shen C, Wu LH, Tang KX, Lin J. CBF-dependent signaling pathway: A key responder to low temperature stress in plants. Crit Rev Biotechnol. 2011;31(2):186–92. doi: 10.3109/07388551.2010.505910. - DOI - PubMed
    1. Sanghera GS, Wani SH, Hussain W, Singh NB. Engineering cold stress tolerance in crop plants. Curr Genomics. 2011;12(1):30–43. doi: 10.2174/138920211794520178. - DOI - PMC - PubMed
    1. Nakashima K, Yamaguchi-Shinozaki K. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant. 2006;126(1):62–71. doi: 10.1111/j.1399-3054.2005.00592.x. - DOI
    1. Chinnusamy V, Zhu J, Zhu J. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007;12(10):444–51. doi: 10.1016/j.tplants.2007.07.002. - DOI - PubMed
    1. Zhang T, Zhao X, Wang W, Pan Y, Huang L, Liu X, et al. Comparative Transcriptome Profiling of Chilling Stress Responsiveness in Two Contrasting Rice Genotypes. PLoS One. 2012;7(8):e43274. doi: 10.1371/journal.pone.0043274. - DOI - PMC - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources