Lindernia brevidens: a novel desiccation‐tolerant vascular plant, endemic to ancient tropical rainforests

Abstract

SummaryA particular adaptation to survival under limited water availability has been realized in the desiccation-tolerant resurrection plants, which tend to grow in a habitat with seasonal rainfall and long dry periods. One of the best-studied examples is Craterostigma plantagineum. Here we report an unexpected finding: Lindernia brevidens, a close relative of C. plantagineum, exhibits desiccation tolerance, even though it is endemic to the montane rainforests of Tanzania and Kenya, where it never experiences seasonal dry periods. L. brevidens has been found exclusively in two fragments of the ancient Eastern Arc Mountains, which were protected from the devastating Pleistocene droughts by the stable Indian Ocean temperature. Analysis of the microhabitat reveals that L. brevidens is found in the same habitat as hygrophilous plant species, which further indicates that the plant never dries out completely. The objective of this investigation was to address whether C. plantagineum and L. brevidens have desiccation-related pathways in common, or whether L. brevidens has acquired novel pathways. A third, closely related, desiccation-sensitive species, Lindernia subracemosa, has been included for comparison. Mechanisms that confer cellular protection during extreme water loss are well conserved between C. plantagineum and L. brevidens, including the interconversion of 2-octulose to sucrose within the two desiccation-tolerant species. Furthermore, transcriptional control regions of desiccation-related genes belonging to the late embryogenesis abundant (LEA) protein family are also highly conserved. We propose that L. brevidens is a neoendemic species that has retained desiccation tolerance through genome stability, despite tolerance being superfluous to environmental conditions.

A Sister Group Contrast Using Untargeted Global Metabolomic Analysis Delineates the Biochemical Regulation Underlying Desiccation Tolerance in Sporobolus stapfianus

“…Whittaker et al (2007) determined that the early increase in carbohydrates is derived from photosynthesis and starch reserves, but that the later accumulation of Suc is derived from phosphorylation of hexose, driven by an increase in Suc phosphate synthase activity and protein. Suc is thought to be derived from photosynthate (starch) stored when plants are hydrated and active, but some DT species, including C. plantagineum, C. wilmsii, and Lindernia brevidens, store 2-octulose when hydrated, which is converted to Suc during dehydration (Bianchi et al, 1991;Cooper and Farrant, 2002;Phillips et al, 2008). Increases in raffinose and stachyose have also been reported for S. stapfianus (Ghasempour et al, 1998) and have often been linked with protection mechanisms in desiccating plant tissues (Farrant, 2007).…”

Plant Desiccation Tolerance and its Regulation in the Foliage of Resurrection “Flowering-Plant” Species

“…Fully hydrated leaves of C. plantagineum contain high levels of the unusual sugar 2-octulose which upon dehydration is converted to sucrose [107]. This interconversion of 2-octulose to sucrose is conserved in the close relative, L. brevidens [106].…”

“…Transformation procedures have been reported for some resurrection species, such as the well-studied dicotyledenous species C. plantagineum [167] and also L. brevidens [168]. The latter species is a more recently described resurrection plant, also from within the family Linderniaceae, and interestingly is found naturally in the montane rainforests of Tanzania and Kenya [106]. However, reliable DNA transformation protocols for other desiccation-tolerant plants have not been reported and development of such methods would be extremely beneficial to the subject area, particularly involving desiccation-tolerant monocotyledonous species.…”

“…Craterostigma plantagineum and Lindernia brevidens Skan. also accumulate sugars in response to desiccation [42,106]. Fully hydrated leaves of C. plantagineum contain high levels of the unusual sugar 2-octulose which upon dehydration is converted to sucrose [107].…”

Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis

“…The small group of angiosperm resurrection plants (about 300 species) displays remarkable habitat and geographic diversity [5]. They are found in dry and desert areas, in more temperate areas with sufficient rain but short periods of drought or/and cold winters, and even in the tropical rainforests of Africa, where humidity is normally high [5,9,10]. Most of the resurrection species are herbaceous plants, but there are also shrubs and trees [4].…”