Abstract

The invertase gene family in plants is composed of two subfamilies of enzymes, namely, acid- and neutral/alkaline invertases (cytosolic invertase, CIN). Both can irreversibly cleave sucrose into fructose and glucose, which are thought to play key roles in carbon metabolism and plant growth. CINs are widely found in plants, but little is reported about this family. In this paper, a comparative genomic approach was used to analyze the CIN gene family in Solanum, including Solanum tuberosum, Solanum lycopersicum, Solanum pennellii, Solanum pimpinellifolium, and Solanum melongena. A total of 40 CINs were identified in five Solanum plants, and sequence features, phylogenetic relationships, motif compositions, gene structure, collinear relationship, and expression profile were further analyzed. Sequence analysis revealed a remarkable conservation of CINs in sequence length, gene number, and molecular weight. The previously verified four amino acid residues (D188, E414, Arg430, and Ser547) were also observed in 39 out of 40 CINs in our study, showing to be deeply conserved. The CIN gene family could be distinguished into groups α and β, and α is further subdivided into subgroups α1 and α2 in our phylogenetic tree. More remarkably, each species has an average of four CINs in the α and β groups. Marked interspecies conservation and collinearity of CINs were also further revealed by chromosome mapping. Exon–intron configuration and conserved motifs were consistent in each of these α and β groups on the basis of in silico analysis. Expression analysis indicated that CINs were constitutively expressed and share similar expression profiles in all tested samples from S. tuberosum and S. lycopersicum. In addition, in CIN genes of the tomato and potato in response to abiotic and biotic stresses, phytohormones also performed. Overall, CINs in Solanum were encoded by a small and highly conserved gene family, possibly reflecting structural and functional conservation in Solanum. These results lay the foundation for further expounding the functional characterization of CIN genes and are also significant for understanding the evolutionary profiling of the CIN gene family in Solanum.

Highlights

  • Sucrose (D-glucopyranosyl-(1–2)-D-fructofuranose), as the principal end product of photosynthesis in higher plants and photosynthetic bacteria, is translocated through the phloem from the source tissue into sink organs as a transport molecule [1,2,3]

  • Neutral/alkaline invertases were identified in Solanum, including S. tuberosum, S. lycopersicum, S. pennellii, S. pimpinellifolium, and S. melongena, which made it possible to perform comparative genomic analysis for the CIN gene family

  • Previous studies have suggested that seven to eleven CINs were identified through a systematic survey in several plant genomes [26,27], whereas these were eight in all the surveyed Solanum species, indicating stability in the number of this small gene family among various plant species

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Summary

Introduction

Sucrose (D-glucopyranosyl-(1–2)-D-fructofuranose), as the principal end product of photosynthesis in higher plants and photosynthetic bacteria, is translocated through the phloem from the source tissue into sink organs as a transport molecule [1,2,3]. Sucrose is either separated into simple hexoses (glucose, galactose, and mannose), or degraded into derivatives, such as deoxy sugar, to supply carbon and energy or to act as signaling molecules for plant growth, development, and stress tolerance [4,5,6,7]. Sucrose is cleaved to hexose by two prime enzymes: sucrose synthase (SuS; EC 2.4.1.13) and invertase (INV; EC 3.2.1.26). The sucrose molecule is cleaved by SuS into uridine diphosphate-glucose and fructose in a reversible manner, whereas it is irreversibly hydrolyzed by INV into fructose and glucose [4,5]. INV widely participates in the regulation of plant growth and development, including controlling reproductive development and responses to stress tolerance [4,7,11,12]. It was found that the activity of cytosolic invertase was indispensable to the growth and reproduction of Arabidopsis thaliana [13]

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