Few organisms are able to withstand desiccation stress; however, desiccation tolerance is widespread among plant seeds. Survival without water relies on an array of mechanisms, including the accumulation of stress proteins such as the late embryogenesis abundant (LEA) proteins. These hydrophilic proteins are prominent in plant seeds but also found in desiccation-tolerant organisms. In spite of many theories and observations, LEA protein function remains unclear. Here, we show that LEAM, a mitochondrial LEA protein expressed in seeds, is a natively unfolded protein, which reversibly folds into a-helices upon desiccation. Structural modeling revealed an analogy with class A amphipathic helices of apolipoproteins that coat low-density lipoprotein particles in mammals. LEAM appears spontaneously modified by deamidation and oxidation of several residues that contribute to its structural features. LEAM interacts with membranes in the dry state and protects liposomes subjected to drying. The overall results provide strong evidence that LEAM protects the inner mitochondrial membrane during desiccation. According to sequence analyses of several homologous proteins from various desiccationtolerant organisms, a similar protection mechanism likely acts with other types of cellular membranes.
Late-embryogenesis abundant (LEA) proteins are hydrophilic proteins that accumulate to a high level in desiccation-tolerant tissues and are thus prominent in seeds. They are expected to play a protective role during dehydration; however, functional evidence is scarce. We identified a LEA protein of group 3 (PsLEAm) that was localized within the matrix space of pea (Pisum sativum) seed mitochondria. PsLEAm revealed typical LEA features such as high hydrophilicity and repeated motifs, except for the N-terminal transit peptide. Most of the highly charged protein was predicted to fold into amphiphilic a-helixes. PsLEAm was expressed during late seed development and remained in the dry seed and throughout germination. Application of the stress hormone abscisic acid was found to reinduce the expression of PsLEAm transcripts during germination. PsLEAm could not be detected in vegetative tissues; however, its expression could be reinduced in leaves by severe water stress. The recombinant PsLEAm was shown to protect two mitochondrial matrix enzymes, fumarase and rhodanese, during drying in an in vitro assay. The overall results constitute, to our knowledge, the first characterization of a LEA protein in mitochondria and experimental evidence for a beneficial role of a LEA protein with respect to proteins during desiccation.Late-embryogenesis abundant (LEA) proteins are overwhelmingly hydrophilic proteins that accumulate to high levels in the latter stages of seed maturation and disappear following germination (Galau et al., 1986). While almost ubiquitous in the plant kingdom, data mining has revealed the widespread occurrence of LEA proteins in prokaryotes and eucaryotes (GarayArroyo et al., 2000). Historically clustered in five main groups based on primary structure analysis (Dure et al., 1989;Cuming, 1999), the LEA protein classification was recently reexamined using statistically based bioinformatic tools (Wise, 2003).LEA protein expression, which often appears abscisic acid (ABA) dependent, can also occur in vegetative tissues subjected to water deficit associated with drought, salt, or cold stress (for review, see Ingram and Bartels, 1996;Thomashow, 1998;Cuming, 1999). Both the pattern of expression and the structural features of LEA proteins suggest a general protective role in desiccation tolerance (Ingram and Bartels, 1996;Cuming, 1999). This hypothesis was recently supported by the discovery of a LEA protein in an anhydrobiotic nematode (Browne et al., 2002) as well as by the sensitization to desiccation induced by mutational inactivation of LEA genes in the prokaryote Deinococcus radiodurans (Battista et al., 2001). In view of the apparent lack of well-ordered tertiary structure of LEA proteins preventing their use as catalysts, several mechanisms have been proposed to relate their structural features to the protection of cellular structures required by a dehydrated state: water replacement, ion sequestering, macromolecules, and membrane stabilization (Close, 1996(Close, , 1997Cuming, 1999). Experimentally, sev...
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