LEA_1 domain-containing proteins constitute a class of late-embryogenesis-abundant proteins that are highly hydrophilic and predominantly accumulate in mature seeds. Though LEA_1 proteins have been proven to be essential for seed desiccation tolerance and longevity, little information is available on their roles in non-seed storage organs. In this study, a first genome-wide characterization of the LEA_1 gene family was conducted in tigernut (Cyperus esculentus L., Cyperaceae), whose underground tubers are desiccation tolerant with a moisture content of less than 6%. Five family members identified in tigernut are comparative to four to six found in seven other Cyperaceae plants, but relatively more than three reported in Arabidopsis. Further comparison of 125 members from 29 plant species supports early divergence of the LEA_1 family into two phylogenetic groups before angiosperm radiation, and gene expansion in tigernut was contributed by whole-genome duplications occurring after the split with the eudicot clade. These two phylogenetic groups could be further divided into six orthogroups in the momocot clade, five of which are present in tigernut and the remaining one is Poaceae specific. Frequent structural variation and expression divergence of paralogs were also observed. Significantly, in contrast to seed-preferential expression of LEA_1 genes in Arabidopsis, rice, and maize, transcriptional profiling and qRT-PCR analysis revealed that CeLEA1 genes have evolved to predominantly express in tubers, exhibiting a seed desiccation-like accumulation during tuber development. Moreover, CeLEA1 transcripts in tubers were shown to be considerably more than that of their orthologs in purple nutsedge, another Cyperaceae plant producing desiccation-sensitive tubers. These results imply species-specific activation and key roles of CeLEA1 genes in the acquisition of desiccation tolerance of tigernut tubers as observed in orthodox seeds. Our findings not only improve the understanding of lineage-specific evolution of the LEA_1 family, but also provide valuable information for further functional analysis and genetic improvement in tigernut.
