Analysis of Cyperus esculentus SMP family genes reveals lineage-specific evolution and seed desiccation-like transcript accumulation during tuber maturation

Seed maturation proteins (SMPs) represent a class of late embryogenesis-abundant proteins that are highly hydrophilic and abundant in mature seeds. Although it has been proven that SMPs are indispensable for the desiccation resistance of orthodox seeds, information on their putative roles in the desiccation resistance of non-seed storage organs is still scarce. This study presents a first transcriptome-based characterization of SMP family genes in tigernut (Cyperus esculentus L., Cyperaceae), whose underground tubers represent a unique system that contains a considerably low moisture content of less than 10% without affecting the sprouting capability. Five family members identified from the full-length tigernut transcriptome are relatively more than four found in the genome of Carex littledalei, another Cyperaceae plant. Moreover, 69 family genes were also identified from 15 representative plant species and comparative genomics analysis supports the monogenic origin of this special family as well as lineage-specific evolution after monocot-eudicot split. In the Cyperaceae lineage, four clades present in the last common ancestor of tigernut and C. littledalei, which represent four out of 11 orthogroups proposed in this study, are more likely to result from transposed and dispersed duplications. In contrast to seed- or embryo-preferential expression of SMP genes in seed-bearing plants (e.g. rice and maize), transcriptional profiling and qRT-PCR analysis showed that most CeSMP genes are predominantly expressed in late stages of developmental tigernut tubers, negatively correlating with the moisture content. This seed desiccation-like accumulation of CeSMP transcripts during tuber maturation implies their putatively important roles in the desiccation resistance of tigernut tubers as observed in orthodox seeds. These findings not only improve the knowledge on lineage-specific evolution of the SMP gene family, but also provide valuable information for further functional analysis and genetic improvement in tigernut.