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Tropical Plant Biology

, Volume 12, Issue 3, pp 158–173 | Cite as

Evolution and Expression Analysis of Starch Synthase Gene Families in Saccharum spontaneum

  • Panpan Ma
  • Yuan Yuan
  • Qiaochu Shen
  • Qing Jiang
  • Xiuting Hua
  • Qing Zhang
  • Muqing Zhang
  • Ray Ming
  • Jisen ZhangEmail author
Article
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Abstract

Starch is one of two crucial products of photosynthetic carbon-assimilation and mainly functions as the unit of energy storage in most crops such as rice, maize and sorghum, whereas interestingly in sugarcane that unit of energy storage is sucrose. Mature sugarcane stalk tissue has a very large apoplastic volume and contains nearly 700 mM sucrose—which is among the highest recorded sucrose concentrations in plant tissue. We identified 9 genes of starch synthases (SSs) related to the starch synthesis pathway in the genome of S. spontaneum. Based on gene structure and phylogenetic analysis, SSs genes were clustered into five clades and were relatively conserved. In S. spontaneum, the SS is a very ancient gene family, in which, SSIIIa and SSIIIb originated from the ρ-whole genome duplications (WGDs), SSIIb and SsIIc originated from gene duplication after the split of monocots and dicots; GBSSI and GBSSII in Clade V and SSIIa in Clade II were retained from the ε-WGD, and the remaining two SSs (SSI and SSIV) were retained from the very ancient gene duplication event about 355–389 million year ago (Mya). In addition, we found all SS genes were under the influence of strong purification with a Ka/Ks ratio of less than 0.5 in S. spontaneum. In the 5 families, SSIIIa, SSIIb and GBSSII had relatively predominant expression levels in all the examined tissues from the two Saccharum species, indicating the three genes were the fundamental members in the non-storage tissues, leaf or stem, which is in agreement with previous studies. Interestingly, the expression levels of SSs in stems showed significantly higher values in S. spontenum than in S. officinarum at pre-mature and mature stages. These results were negatively correlated with the sucrose levels between the two Saccharum species. At the pre-mature and mature stages, the sucrose contents in stems from S. officinarum were much higher than in stems from S. spontenum, suggesting that SSs involved in the differential of carbohydrate metabolism between the two Saccharum species. Besides, the expression of SSs displayed a clearly consistent trend in line with normal distribution under the diurnal rhythms of S. spontaneum. Moreover, the expression pattern of SSIIIa, SSIIb and GBSSII displayed a clearly consistent trend in both Saccharum species and in maize, rice, which was in accordance with photosynthetic intensity across leaf gradients. This result suggested the functional constraints for the SSs gene family in Gramineae. Our results are valuable for further functional analysis of SSs genes and provided the foundation for carbohydrate metabolism in sugarcane.

Keywords

Gene expression Gene evolution Saccharum spontaneum Starch synthetases 
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Notes

Acknowledgements

This project was supported by grants from the 863 program (2013AA100604), NSFC (31201260, 31760413 and 31660420), Science and Technology Major Project of Guangxi (AA17202025) and Fujian Provincial Department of Education (No. JA12082). We are grateful for editing the language of Irene Lavagi.

Authors’ Contributions

Jisen Zhang designed the experiments. Jisen Zhang and Panpan Ma conceived the study. Panpan Ma, Yuan Yuan, Qiaochu Shen, Qing Jiang, Xiuting Hua, Qing Zhang, Muqing Zhang, Ray Ming performed the experiments and analyzed the data. Panpan Ma and Jisen Zhang wrote the manuscript. All authors read and approved the final article.

Compliance with Ethical Standards

Conflict of Interests

The authors declare no competing financial interests.

Supplementary material

12042_2019_9225_MOESM1_ESM.docx (17 kb)
Table S1 Comparison of the allelic characteristics of the starch synthetases genes in S. spontaneum. The identity value is the similarity of protein sequences in sugarcane aligned to corresponding orthologs in sorghum. (DOCX 16 kb)
12042_2019_9225_Fig8_ESM.png (175 kb)
Fig. S1

The calculation of substitution rates of homologues of starch synthetases genes between S.spontaneum and S. bicolor. (PNG 174 kb)

12042_2019_9225_MOESM2_ESM.tif (70 kb)
High Resolution Image (TIF 70 kb)
12042_2019_9225_Fig9_ESM.png (1.2 mb)
Fig. S2

The comparison of allelic gene structure of starch synthetases in S. spontaneum. Gene structure starts from translation start sites to stop sites. Diagram is drawn to scale. Exons are represented by boxes and introns as lines. (PNG 1236 kb)

12042_2019_9225_MOESM3_ESM.tif (240 kb)
High Resolution Image (TIF 239 kb)
12042_2019_9225_Fig10_ESM.png (290 kb)
Fig. S3

The expression of SpSSIIa, SoSSIIa, and SoGBSSII in different tissues by qRT-PCR. JY, leaf roll; ZY: leaf; J6: stem 6; J9: stem 9. The expression values from the RNA-seq database are marked by the blue bar based on FPKM values on the left hand side, and expression levels from qRT-PCR experiments are marked by orange dashed line using the scale on the right hand side based on the relative values to value of stem 9 in S. spontaneum and stem 15 in S. officinarum, relatively. (PNG 290 kb)

12042_2019_9225_MOESM4_ESM.tif (111 kb)
High Resolution Image (TIF 111 kb)
12042_2019_9225_Fig11_ESM.png (173 kb)
Fig. S4

The starch content of leaf and stem in seedling from sorghum and three Saccharum species. (PNG 173 kb)

12042_2019_9225_MOESM5_ESM.tif (54 kb)
High Resolution Image (TIF 54 kb)
12042_2019_9225_MOESM6_ESM.xlsx (110 kb)
Additional file 1 The gene information of starch synthases from different species collected based on previous studies, including 4 dicots, 6 monocots, A. trichopoda and 3 outgroup species. (XLSX 110 kb)
12042_2019_9225_MOESM7_ESM.fasta (21 kb)
Additional file 2 The gene sequence information of nine starch synthases and their alleles in S. spontaneum. (FASTA 21 kb)

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Panpan Ma
    • 1
  • Yuan Yuan
    • 2
  • Qiaochu Shen
    • 1
  • Qing Jiang
    • 1
  • Xiuting Hua
    • 1
  • Qing Zhang
    • 1
  • Muqing Zhang
    • 3
  • Ray Ming
    • 1
    • 4
  • Jisen Zhang
    • 1
    Email author
  1. 1.Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Crop ScienceFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.College of Life SciencesFujian Normal UniversityFuzhouChina
  3. 3.Guangxi Key Lab for Sugarcane BiologyGuangxi UniversityNanningChina
  4. 4.Department of Plant BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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