Research

Background

A significant increase of the global temperature has been monitored during the last century and a further rise by 1-4°C until the end of this century is proposed, where 90% of this global warming is attributed to the increase of anthropogenic greenhouse gases [1]. The expected temperature increase and climate changes will have far-reaching consequences on the productivity of crop plants, and thus on the food supply all over the world [2]. Although plants have developed versatile adaptation and tolerance mechanisms to minimize perturbing effects to a certain extent, major losses of the crop productivity are caused by high temperatures which frequently appear in combination with other abiotic or biotic stressors [3]. In view of the expected climate changes, sustainable crop reproduction essentially requires the availability of varieties with improved performance under less favourable environmental conditions in general. To this end, the exploration of the genetic and molecular background of stress response mechanisms and the understanding of the physiological bases of stress tolerance in naturally occurring tolerant plants will accelerate the breeding of tolerant varieties by increasing the efficiency of screenings [4].

Exposure to higher temperatures was shown to disturb plant reproduction processes in a number of crop plants, causing failure of male gametophyte development and consequent infertility [5][6]. In tomato, pollen development starts inside the anther 7-8 days before anthesis, when pollen mother cells undergo meiosis to form tetrads of microspores enclosed in a callose wall. The microspores are freed by callase, an enzyme produced by a layer of tapetum cells which also feeds the developing microspores. In the later stages of pollen development the tapetum disintegrates into the locular fluid surrounding the developing microspores. During further development, microspores undergo an asymmetric mitosis to form a bicellular pollen grain composed of a large vegetative cell and a small generative cell. The vegetative cell will form the pollen tube, while the generative cell, engulfed in the cytoplasm of the vegetative cell, will undergo a second mitosis to form two sperm cells.

Microsporogenesis (spore formation) and male gametogenesis (sperm cell formation) are temperature sensitive. Exposure to prolonged moderate temperatures (~30°C) or to short-term heat stress (HS) conditions (e.g. 2 h at 43-45°C) have severe influences on anther and pollen development by affecting both, the number of pollen and their quality, leading to male sterility and yield reduction [5][6]. Thus, plant reproduction under HS depends on the capacity of the developing pollen grains to withstand high temperature damages and the synchronized and proper development of the anther tissues [6][7]. Nevertheless, data on the molecular basis for pollen HS-sensitivity, PTT, and the impact of HS on anther tissues are very limited. Only recently it was demonstrated that specific heat shock transcription factors (Hsf), chaperones and genes involved in hormone signalling and carbohydrate metabolism are involved in developing pollen HSR [8][9]. For several of these genes, higher basal expression levels were detected in non-stressed microspores of a heat-tolerant genotype compared with a heat-sensitive genotype, marking them as important for microspore thermotolerance [8][9], but the underlying mechanisms remain to be explored.

In general, HS interferes with the cellular homeostasis by influencing fundamental processes, such as membrane fluidity and permeability, protein synthesis and folding, cell division, signalling and metabolic pathways in all organisms [10]. The evolution of adaptive mechanisms for efficient protection of the structural and functional cellular integrity was essential for survival under permanently changing temperature conditions. In addition to the evolved basal thermotolerance, response mechanisms induced by short-term sub-lethal temperatures can enhance the protection at further elevating temperatures, a phenomenon referred as acquired thermotolerance (ATT) [11]. A central aspect of the cellular HSR is the transient reprogramming of gene expression by activation of HS-inducible genes and the synthesis of heat shock proteins (Hsps). Most of these proteins are molecular chaperones, which bind partially unfolded proteins to protect them from denaturation occurring under proteotoxic stress conditions [10][11][12][13]. Chaperones are found in all cellular compartments and organelles and perform essential housekeeping functions for maintenance of protein homeostasis under normal growth conditions. They assist folding and targeting of newly synthesized proteins to their functional states and contribute to the cellular protein quality control by guiding misfolded or aggregated proteins for degradation [13][14][15]. Other HS-induced genes are involved more specifically in distinct thermotolerance-related acclimation processes, i.e. protection from oxidative stress, signalling of phytohormones, or synthesis of osmoprotective metabolites11. Altogether, in response to higher temperatures the expression of more than thousand genes can be assumed to be affected [16].

Higher temperatures induce the activation of Hsfs in all eukaryotes. In plants, Hsfs form a gene family of a large complexity with more than 20 members [17]. Hsfs bind to conserved palindromic sequence motifs (HS elements, HSE) in promoter regions of target genes [18], and regulate expression by cooperating in a dynamic network between distinct family members [19]. Although only few Hsfs are investigated in detail, specific functions in stress response and development rather than redundancy can be attributed to individual members of the plant Hsf family [20]. In addition, during repeated cycles of HS and recovery the activity and composition of the cellular Hsf network is dynamically controlled by factor-specific interactions with distinct chaperones from the Hsp70, Hsp90 and small Hsp families [21]. Thus, a versatile regulatory system based on the two central networks required for the efficient adaptation under permanently changing temperature conditions exists, which is not yet understood in detail. The above introduced acquired thermotolerance lasts for only short periods if it depends on the half-life of stress-induced proteins, RNAs, and metabolites, but lasts much longer if it is based on modifications to chromatin structure that affect gene expression [22]. Such "epigenetic modifications" include DNA methylation and histone modification and are mitotically, and sometimes even meiotically (i.e. trans-generationally), heritable [23]. Hence, acquisition of PTT is expected to depend on such processes as well.

Tomato production is important for the fresh fruit market and for industrial processing all over the world [24]. Thus, in view of the global warming, pollen viability and male sterility became major traits for breeding heat-tolerant cultivars. Comparative studies on heat-sensitive and heat-tolerant tomato cultivars over the last decade have provided first insights into the complexity of physiological and metabolic changes associated with pollen viability and fruit setting at higher temperatures [25]. Recent high throughput transcriptomic approaches and proteomic studies indicate that components of the HSR system are genetically connected to the developmental program during all stages of pollen maturation [8][9][26]. Despite this progress, the molecular basis for the high temperature sensitivity of developing pollen grains and the mechanisms contributing to an increased thermotolerance in heat-tolerant genotypes are still poorly understood. The existence of other, yet unknown cofactors or mechanisms have to be assumed to contribute to PTT. Consequently, the objective of the proposed research program is to establish a network of excellent research groups, which will focus on the characterization of factors participating in mechanisms leading to HS-induced infertility on the one hand, and higher PTT on the other. The participants in the project are chosen so as to define a set of BIOMARKERS indicating POLLEN-THERMOTOLERANCE (PTT) already at early vegetative growth stages, similar to that found for drought respons [27]. Thus, University and Agricultural Research Institute as well as Industry research groups are involved in the project. The crop plant tomato is chosen as an initial plant model that will be used by all participating groups.

References

  • [1] Mittler R (2006) Trends Plant Sci. 11:15 19.
  • [2] Tardieu F, Tuberosa R (2010) Curr. Opin. Plant Biol. 13:206-212.
  • [3] Peet et al. (1998) Plant Cell Environ. 21:225-231.
  • [4] Monterroso VA, Wien HC. (1990) J. American Soc. Horticult. Sci. 115:631-634.
  • [5] Erickson AN, Markhart AH. (2002) Plant, Cell Environ. 25:123-130.; Sakata et al. (2000) J. Plant Res. 113:395-402.; Pressman et al. (2007) Plant Stress 1:216-227
  • [6] Kim et al. (2001) J Plant Res. 114:301-307.
  • [7] Jain et al. (2007) Planta 227:67-79;
  • [8] Firon et al. (2006) Scient Hort. 109:212-217.
  • [9] Frank et al. (2009) J Exp Bot. 60:3891-3908.
  • [10] Giorno et al. (2010) J Exp Bot. 61:453-462.
  • [11] Nover L. (ed.) (1991) Heat shock response. CRC Press, Boca Raton
  • [12] Kotak et al. (2007) Curr. Opin. Plant Biol. 10:310-316.
  • [13] Bösl et al. (2006) J Struct Biol. 156:139-148.
  • [14] Morimoto RI. (2008). Genes Dev. 22: 1427-1438.
  • [15] Young et al. (2004) Nat Rev Mol Cell Biol. 5:781-791.; Mirus O, Schleiff E. (2009) Endocytobiosis Cell Res. 19:31-50. Lee et al. (2010) Plant Cell 21:3984-4001.
  • [16] Larkindale J, Vierling, E. (2008) Plant Physiol. 146:748-761.
  • [17] Nover L, Bharti K, Döring P, Mishra SK, Ganguli A and Scharf KD (2001) Cell Stress Chap. 6:177-189.
  • [18] Pelham HRB (1982) Cell 30:517-528.
  • [19] Baniwal et al. (2004) J Biosci. 29:471-487.
  • [20] von Koskull-Döring et al. (2007) Trends Plant Sci. 12:452-457.
  • [21] Port et al. (2004) Plant Physiol. 135:1457-1470.; Yamada et al. (2007) J Biol Chem. 282:37794-37804.; Meiri D, Breiman A. (2009) Plant J. 59:387-399.
  • [22] Chinnusami V, Zhu JK. (2009) Curr. Opin. Plant Biol. 12:133-139.
  • [23] Whittle et al.. (2009) Botany 87:650-657
  • [24] Barone et al. (2009) Curr. Genomics. 10:1-9.
  • [25] Pressman et al. (2002) Ann. Bot. 90:631-636.; Pressman et al. (2006) J Hort Sci Biotechnol. 81:341-348.
  • [26] Sheoran et al. (2007) J Exp Bot. 58:3525-3535.
  • [27] Chenu et al. (2009) Genetics 183:1507-1523.

 

 

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