The Metabolic Basis of Pollen Thermo-Tolerance: Perspectives for Breeding

Crop production is highly sensitive to elevated temperatures. A rise of a few degrees above the optimum growing temperature can lead to a dramatic yield loss. A predicted increase of 1–3 degrees in the twenty first century urges breeders to develop thermo-tolerant crops which are tolerant to high temperatures. Breeding for thermo-tolerance is a challenge due to the low heritability of this trait. A better understanding of heat stress tolerance and the development of reliable methods to phenotype thermo-tolerance are key factors for a successful breeding approach. Plant reproduction is the most temperature-sensitive process in the plant life cycle. More precisely, pollen quality is strongly affected by heat stress conditions. High temperature leads to a decrease of pollen viability which is directly correlated with a loss of fruit production. The reduction in pollen viability is associated with changes in the level and composition of several (groups of) metabolites, which play an important role in pollen development, for example by contributing to pollen nutrition or by providing protection to environmental stresses. This review aims to underline the importance of maintaining metabolite homeostasis during pollen development, in order to produce mature and fertile pollen under high temperature. The review will give an overview of the current state of the art on the role of various pollen metabolites in pollen homeostasis and thermo-tolerance. Their possible use as metabolic markers to assist breeding programs for plant thermo-tolerance will be discussed.

[1]  Zhiqing Jin,et al.  Possible correlation between high temperature-induced floret sterility and endogenous levels of IAA, GAs and ABA in rice (Oryza sativa L.) , 2007, Plant Growth Regulation.

[2]  Francisco Marco,et al.  Involvement of polyamines in plant response to abiotic stress , 2006, Biotechnology Letters.

[3]  P. V. Vara Prasad,et al.  FRUIT NUMBER IN RELATION TO POLLEN PRODUCTION AND VIABILITY IN GROUNDNUT EXPOSED TO SHORT EPISODES OF HEAT STRESS , 1999 .

[4]  A. H. Markhart,et al.  Flower developmental stage and organ sensitivity of bell pepper (Capsicum annuum L.) to elevated temperature , 2002 .

[5]  M. Wolters-Arts,et al.  Ethylene regulates the timing of anther dehiscence in tobacco , 2003, Planta.

[6]  I. Singh,et al.  Physiological and Molecular Effects of 24-Epibrassinolide, a Brassinosteroid on Thermotolerance of Tomato , 2005, Plant Growth Regulation.

[7]  M. Peet,et al.  The effect of high temperature and high atmospheric CO2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination. , 2001, Physiologia plantarum.

[8]  D. Geelen,et al.  The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms , 2013, Plant, cell & environment.

[9]  K. S. Labana,et al.  Male sterility in Indian mustard (Brassica juncea (L.) Coss.) — a biochemical characterization , 1984, Theoretical and Applied Genetics.

[10]  C. Clément,et al.  Sucrose and starch catabolism in the anther of Lilium during its development: a comparative study among the anther wall, locular fluid and microspore/pollen fractions , 2007, Planta.

[11]  Shaoling Zhang,et al.  The effect of temperature, polyamines and polyamine synthesis inhibitor on in vitro pollen germination and pollen tube growth of Prunus mume , 2004 .

[12]  Giovanni Agati,et al.  Flavonoids as antioxidants in plants: location and functional significance. , 2012, Plant science : an international journal of experimental plant biology.

[13]  Md. Mahabubul Alam,et al.  Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants , 2013, International journal of molecular sciences.

[14]  C. Clément,et al.  Pollen vacuoles and their significance , 2011, Planta.

[15]  K. Ljung,et al.  Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. , 2013, The Plant journal : for cell and molecular biology.

[16]  O. Chambliss,et al.  Fruit Set, Pollen Fertility, and Combining Ability of Selected Tomato Genotypes under High- temperature Field Conditions , 1991 .

[17]  B. S. Ahloowalia,et al.  Molecular techniques in crop improvement , 2002 .

[18]  S. Savaldi-Goldstein,et al.  Brassinosteroids in growth control: how, when and where. , 2013, Plant science : an international journal of experimental plant biology.

[19]  J. Browse,et al.  The Critical Requirement for Linolenic Acid Is Pollen Development, Not Photosynthesis, in an Arabidopsis Mutant. , 1996, The Plant cell.

[20]  Takayuki Sasaki,et al.  Quality control of photosystem II: impact of light and heat stresses , 2008, Photosynthesis Research.

[21]  P. Hazra,et al.  Genetics of heat tolerance for floral and fruit set to high temperature stress in tomato (Lycopersicon esculentum Mill.). , 2008 .

[22]  A. Stephenson,et al.  Effects of Temperature During Microsporogenesis on Pollen Performance in Cucurbita pepo L. (Cucurbitaceae) , 1998, International Journal of Plant Sciences.

[23]  S. Henikoff,et al.  High-throughput screening for induced point mutations. , 2001, Plant physiology.

[24]  S. Sato,et al.  Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. , 2006, Annals of botany.

[25]  T. Roitsch,et al.  Source-sink regulation by sugar and stress. , 1999, Current opinion in plant biology.

[26]  T. Stocker,et al.  Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A Special Report of Working Groups I and II of IPCC Intergovernmental Panel on Climate Change , 2012 .

[27]  K. Siddique,et al.  Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. , 2013, Functional plant biology : FPB.

[28]  A. R. Reddy,et al.  Mulberry Leaf Metabolism under High Temperature Stress , 2001, Biologia Plantarum.

[29]  R. J. Baker,et al.  Estimation of heritability and prediction of selection response in plant populations , 1991 .

[30]  E. Pressman,et al.  The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. , 2002, Annals of botany.

[31]  N. Murata,et al.  Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. , 2011, Plant, cell & environment.

[32]  Mary M. Peet,et al.  Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress , 2000 .

[33]  R. Tuberosa,et al.  Effect of Abscisic Acid on Pollen Germination and Tube Growth of Maize Genotypes1 , 1993 .

[34]  M. Endo,et al.  Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants , 2007, Molecular Genetics and Genomics.

[35]  D. Garrido,et al.  Requirement of polyamines for in-vitro maturation of the mid-binucleate pollen of Nicotiana tabacum , 1993 .

[36]  S. Pollastri,et al.  Flavonoids as Antioxidants and Developmental Regulators: Relative Significance in Plants and Humans , 2013, International journal of molecular sciences.

[37]  G. Acquaah Principles of plant genetics and breeding , 2006 .

[38]  M. Kojima,et al.  Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. , 2006, The Plant journal : for cell and molecular biology.

[39]  A. Hall,et al.  Proline Content of the Anthers and Pollen of Heat-Tolerant and Heat-Sensitive Cowpea Subjected to Different Temperatures , 1989 .

[40]  K. Omasa,et al.  Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. , 2002, Annals of botany.

[41]  D. Funck,et al.  Proline metabolism and transport in plant development , 2010, Amino Acids.

[42]  R. Malmberg,et al.  Do Polyamines Have Roles in Plant Development , 1989 .

[43]  M. Sedgley,et al.  Development Anatomy in Wheat of Male Sterility Induced by Heat Stress, Water Deficit or Abscisic Acid , 1984 .

[44]  E. Heuvelink,et al.  Influence of sub-optimal temperature on tomato growth and yield: a review , 2005 .

[45]  A. Hall,et al.  HEAT INJURY DURING FLORAL DEVELOPMENT IN COWPEA (VIGNA UNGUICULATA, FABACEAE) , 1992 .

[46]  R. R. Johnson,et al.  High Temperature Stress and Pollen Viability of Maize 1 , 1980 .

[47]  Mike J. May,et al.  Glutathione homeostasis in plants: implications for environmental sensing and plant development , 1998 .

[48]  S. Tabata,et al.  Ultrastructural characterization of exine development of the transient defective exine 1 mutant suggests the existence of a factor involved in constructing reticulate exine architecture from sporopollenin aggregates. , 2008, Plant & cell physiology.

[49]  R. Mittler,et al.  Abiotic stress, the field environment and stress combination. , 2006, Trends in plant science.

[50]  M. Wolters-Arts,et al.  Lipids are required for directional pollen-tube growth , 1998, Nature.

[51]  Y. Mo,et al.  Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[52]  T. Tsukaguchi,et al.  Ultrastructural study on degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat stress , 2001, Sexual Plant Reproduction.

[53]  Sheng-Wei Zhang,et al.  Altered Architecture and Enhanced Drought Tolerance in Rice via the Down-Regulation of Indole-3-Acetic Acid by TLD1/OsGH3.13 Activation1[C][W] , 2009, Plant Physiology.

[54]  V. Kakani,et al.  Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. , 2005, Annals of botany.

[55]  J. Audran,et al.  Anther wall layers control pollen sugar nutrition inLilium , 1995, Protoplasma.

[56]  K. Asano,et al.  Gibberellin Regulates Pollen Viability and Pollen Tube Growth in Rice[W] , 2007, The Plant Cell Online.

[57]  Stefanie Sultmanis,et al.  High temperature stress and its effect on pollen development and morphological components of harvest index in the C3 model grass Brachypodium distachyon , 2013, Journal of experimental botany.

[58]  M. Margis-Pinheiro,et al.  Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection , 2012, Genetics and molecular biology.

[59]  I. Nishiyama,et al.  Effects of High Temperature on the Development of Pollen Mother Cells and Microspores in Barley Hordeum vulgare L. , 2000, Journal of Plant Research.

[60]  R. G. Hurd,et al.  The Effect of Early Low Temperature Treatment on the Yield of Single-Inflorescence Tomatoes , 1970 .

[61]  M. de Maeyer,et al.  Understanding the Role of Defective Invertases in Plants: Tobacco Nin88 Fails to Degrade Sucrose1[W] , 2013, Plant Physiology.

[62]  U. Feller,et al.  Heat sensitivity of Rubisco, Rubisco activase and Rubisco binding protein in higher plants , 2004, Acta Physiologiae Plantarum.

[63]  A. Gupta,et al.  Abiotic stress tolerance in plants , 2015 .

[64]  M. Al-Whaibi Plant heat-shock proteins: A mini review , 2011 .

[65]  Mary M. Peet,et al.  Comparing heat stress effects on male‐fertile and male‐sterile tomatoes , 1998 .

[66]  M. Peet,et al.  Formation of parthenocarpic fruit, undeveloped flowers and aborted flowers in tomato under moderately elevated temperatures , 2001 .

[67]  E. Pressman,et al.  Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions , 2012, AoB PLANTS.

[68]  S. Tachibana,et al.  Ameliorative effect of polyamines on the high temperature inhibition of in vitro pollen germination in tomato (Lycopersicon esculentum Mill.) , 1999 .

[69]  L. M. Mazorra Brassinosteroid action and its relation with heat stress mechanisms in plants , 2011 .

[70]  Yuyang Wang,et al.  Proteomics Analysis of Alfalfa Response to Heat Stress , 2013, PloS one.

[71]  F. Turano,et al.  Gamma Aminobutyric Acid (GABA) and Plant Responses to Stress , 2000 .

[72]  B. Dawson,et al.  INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE (IPCC) , 2008 .

[73]  M. Yusuf,et al.  Polyamines: potent modulators of plant responses to stress , 2013 .

[74]  Patrick Achard,et al.  Gibberellin signaling in plants , 2013, Development.

[75]  Taylor,et al.  white anther: A petunia mutant that abolishes pollen flavonol accumulation, induces male sterility, and is complemented by a chalcone synthase transgene , 1999, Plant physiology.

[76]  J. Rudich,et al.  Genotypic Variation for Sensitivity to High Temperature in the Tomato: Pollination and Fruit Set , 1977, Botanical Gazette.

[77]  P. Prasad,et al.  High night temperature decreases leaf photosynthesis and pollen function in grain sorghum. , 2011, Functional plant biology : FPB.

[78]  J. Pichtel,et al.  Role of proline under changing environments , 2012, Plant signaling & behavior.

[79]  K. Boote,et al.  Effects of season-long high temperature growth conditions on sugar-to-starch metabolism in developing microspores of grain sorghum (Sorghum bicolor L. Moench) , 2007, Planta.

[80]  Huei-Mei Chen,et al.  Quantitative trait loci influencing fruit-related characteristics of tomato grown in high-temperature conditions , 2010, Euphytica.

[81]  S. Ishiguro,et al.  The DEFECTIVE IN ANTHER DEHISCENCE1 Gene Encodes a Novel Phospholipase A1 Catalyzing the Initial Step of Jasmonic Acid Biosynthesis, Which Synchronizes Pollen Maturation, Anther Dehiscence, and Flower Opening in Arabidopsis , 2001, The Plant Cell Online.

[82]  B. Koffler,et al.  Glutathione synthesis is essential for pollen germination in vitro , 2011, BMC Plant Biology.

[83]  Markers for breeding heat-tolerant cowpea , 2013, Molecular Breeding.

[84]  R. Creelman,et al.  BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS. , 1997, Annual review of plant physiology and plant molecular biology.

[85]  D. Tan,et al.  Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments. , 2012, Functional plant biology : FPB.

[86]  E. Pressman,et al.  Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response , 2009, Journal of experimental botany.

[87]  T. Roitsch,et al.  Induction of male sterility in plants by metabolic engineering of the carbohydrate supply , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[88]  Y. Mano,et al.  The pathway of auxin biosynthesis in plants. , 2012, Journal of experimental botany.

[89]  A. F. Croes,et al.  Protection of pollen germination from adverse temperatures: a possible role for proline , 1983 .

[90]  M. Jahn,et al.  Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris , 2001 .

[91]  M. M'rani-Alaoui,et al.  Behavior of storage lipids during development and germination of olive (Olea europaea L.) pollen , 2003, Protoplasma.

[92]  V. Shulaev,et al.  When Defense Pathways Collide. The Response of Arabidopsis to a Combination of Drought and Heat Stress1[w] , 2004, Plant Physiology.

[93]  N. Gruda,et al.  Influence of High Temperatures on Gas Exchange Rate and Growth of Eight Tomato Cultivars under Controlled Heat Stress Conditions , 2009 .

[94]  K. L. Bokszczanin,et al.  Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance , 2013, Front. Plant Sci..

[95]  A. Wahid,et al.  Heat tolerance in plants: An overview , 2007 .

[96]  L. Karni,et al.  Fructokinase and hexokinase from pollen grains of bell pepper (Capsicum annuum L.): possible role in pollen germination under conditions of high temperature and CO2 enrichment. , 2002, Annals of botany.

[97]  L. H. Allen,et al.  Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress , 2006 .

[98]  Ilha Lee,et al.  Heat Shock Stress Causes Stage-specific Male Sterility in Arabidopsis thaliana , 2001, Journal of Plant Research.

[99]  D. Ort,et al.  How Do We Improve Crop Production in a Warming World? , 2010, Plant Physiology.

[100]  M. Bihamta,et al.  Marker Assisted Selection for Heat Tolerance in Bread Wheat , 2013 .

[101]  V. Rakitin,et al.  Ethylene is Involved in the Control of Male Gametophyte Development and Germination in Petunia , 2011, Journal of Plant Growth Regulation.

[102]  A. Savouré,et al.  Proline: a multifunctional amino acid. , 2010, Trends in plant science.

[103]  V. Sawhney,et al.  Microsporogenesis in the normal and male-sterile stamenIess-2 mutant of tomato (Lycopersicon esculentum) , 1988 .

[104]  N. Sugiyama,et al.  Pollen Quality and Performance in Strawberry Plants Exposed to High-temperature Stress , 2005 .

[105]  E. Pacini Types and meaning of pollen carbohydrate reserves , 1996, Sexual Plant Reproduction.

[106]  K. Kregel,et al.  Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. , 2002, Journal of applied physiology.

[107]  J. Stommel,et al.  Pollen Viability and Fruit Set of Tomato Genotypes under Optimumand High-temperature Regimes , 1995 .

[108]  N. Goto,et al.  Role of gibberellins in the development of floral organs of the gibberellin-deficient mutant, ga1-1, of Arabidopsis thaliana , 1999 .

[109]  R. Knox,et al.  Invertases of Lilium Pollen : Characterization and Activity during In Vitro Germination. , 1984, Plant physiology.

[110]  R. Sairam,et al.  Protective role of antioxidant enzymes under high temperature stress. , 2006, Plant science : an international journal of experimental plant biology.

[111]  D. Honys,et al.  Male gametophyte development and function. , 2006 .

[112]  W. Schapaugh,et al.  Soybean Pollen Anatomy, Viability and Pod Set under High Temperature Stress , 2013 .

[113]  A. Matilla,et al.  How Ethylene Works in the Reproductive Organs of Higher Plants , 2006, Plant signaling & behavior.

[114]  Christophe Clément,et al.  Characteristics of the Photosynthetic Apparatus and CO2-Fixation in the Flower Bud of Lilium. I. Corolla , 1997, International Journal of Plant Sciences.

[115]  Daphne Preuss,et al.  Pollen and Stigma Structure and Function: The Role of Diversity in Pollination , 2004, The Plant Cell Online.

[116]  S. Tachibana,et al.  Suppression of S-adenosylmethionine decarboxylase activity is a major cause for high-temperature inhibition of pollen germination and tube growth in tomato (Lycopersicon esculentum Mill.). , 2002, Plant & cell physiology.

[117]  L. Young,et al.  High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. , 2004, Journal of experimental botany.

[118]  M. Thomson,et al.  Mapping QTL for heat tolerance at flowering stage in rice using SNP markers , 2012 .

[119]  Jitendra P Khurana,et al.  Transcript profiling reveals diverse roles of auxin‐responsive genes during reproductive development and abiotic stress in rice , 2009, The FEBS journal.

[120]  C. Field Managing the risks of extreme events and disasters to advance climate change adaption , 2012 .

[121]  G. Falasca,et al.  Auxin Regulates Arabidopsis Anther Dehiscence, Pollen Maturation, and Filament Elongation[W] , 2008, The Plant Cell Online.

[122]  K. Boote,et al.  Influence of high temperature during pre- and post-anthesis stages of floral development on fruit-set and pollen germination in peanut , 2001 .

[123]  M. Iacobucci,et al.  A null mutation in the first enzyme of flavonoid biosynthesis does not affect male fertility in Arabidopsis. , 1996, The Plant cell.

[124]  C. Foyer,et al.  ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. , 1998, Annual review of plant physiology and plant molecular biology.

[125]  Yunde Zhao,et al.  Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. , 2006, Genes & development.

[126]  B. Ylstra,et al.  Flavonols stimulate development, germination, and tube growth of tobacco pollen. , 1992, Plant physiology.

[127]  M. Trovato,et al.  Proline is required for male gametophyte development in Arabidopsis , 2012, BMC Plant Biology.

[128]  P. Craufurd,et al.  Genetic analysis of heat tolerance at anthesis in rice , 2010 .

[129]  Yi Pan,et al.  Quantitative Trait Loci Associated with Pollen Fertility under High Temperature Stress at Flowering Stage in Rice (Oryza sativa) , 2011 .

[130]  E. Pressman,et al.  Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions , 2006 .

[131]  F. B. Abeles,et al.  Regulation of Ethylene Evolution and Leaf Abscission by Auxin. , 1964, Plant physiology.

[132]  K. Strzałka,et al.  Carotenoids and Environmental Stress in Plants: Significance of Carotenoid-Mediated Modulation of Membrane Physical Properties , 2003, Russian Journal of Plant Physiology.

[133]  J. Reed,et al.  AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana , 2005, Development.

[134]  Bingru Huang,et al.  Carbohydrate Accumulation in Relation to Heat Stress Tolerance in Two Creeping Bentgrass Cultivars , 2000 .

[135]  M. Knight,et al.  Protection against Heat Stress-Induced Oxidative Damage in Arabidopsis Involves Calcium, Abscisic Acid, Ethylene, and Salicylic Acid , 2002, Plant Physiology.

[136]  A. Gómez-Cadenas,et al.  Metabolomics as a Tool to Investigate Abiotic Stress Tolerance in Plants , 2013, International journal of molecular sciences.

[137]  M. Franceschetti,et al.  Polyamine biosynthesis and control of the development of functional pollen in kiwifruit. , 2010, Plant physiology and biochemistry : PPB.

[138]  W. Vriezen,et al.  The role of auxin and gibberellin in tomato fruit set. , 2009, Journal of experimental botany.

[139]  D. Los,et al.  Heat stress: an overview of molecular responses in photosynthesis , 2008, Photosynthesis Research.

[140]  C. Frova,et al.  Quantitative trait loci (QTLs) for pollen thermotolerance detected in maize , 1994, Molecular and General Genetics MGG.

[141]  G. Kuo,et al.  Gene Action and Heritability of High-temperature Fruit Set in Tomato Line CL5915 , 2002 .

[142]  Zhi-ming Wei,et al.  Effects of specific expression of iaaL gene in tobacco tapetum on pollen embryogenesis , 1997, Science in China Series C: Life Sciences.

[143]  Bhaskar Gupta,et al.  Plant polyamines in abiotic stress responses , 2013, Acta Physiologiae Plantarum.

[144]  J. Patrick,et al.  High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit , 2011, Journal of experimental botany.

[145]  T. Takabe,et al.  Abiotic stress tolerance in plants , 2006 .

[146]  S. Tachibana,et al.  The early increase of S-adenosylmethionine decarboxylase activity is essential for the normal germination and tube growth in tomato (Lycopersicon esculentum Mill.) pollen , 2001 .

[147]  Faye M. Rosin,et al.  RNA Interference Silencing of Chalcone Synthase, the First Step in the Flavonoid Biosynthesis Pathway, Leads to Parthenocarpic Tomato Fruits[C] , 2007, Plant Physiology.

[148]  M. Peet,et al.  Determining critical pre- and post-anthesis periods and physiological processes in Lycopersicon esculentum Mill. exposed to moderately elevated temperatures. , 2002, Journal of experimental botany.

[149]  I. Vasil Developing Cell and Tissue Culture Systems for the Improvement of Cereal and Grass Crops , 1987 .

[150]  G. Galiba,et al.  Glutathione as an Antioxidant and Regulatory Molecule in Plants Under Abiotic Stress Conditions , 2009, Journal of Plant Growth Regulation.

[151]  Charles L. Guy,et al.  Exploring the Temperature-Stress Metabolome of Arabidopsis1[w] , 2004, Plant Physiology.

[152]  E. Pressman,et al.  Variations in Carbohydrate Content and Sucrose-Metabolizing Enzymes in Tomato (Solanum lycopersicum L.) Stamen Parts during Pollen Maturation , 2012 .

[153]  P. Hazra,et al.  Breeding tomato tolerant to high temperature stress. , 2009 .

[154]  R. Parish,et al.  Tapetal development and abiotic stress: a centre of vulnerability. , 2012, Functional plant biology : FPB.

[155]  C. Clément,et al.  Floral organ growth and carbohydrate content during pollen development in Lilium , 1996 .

[156]  E. G. Lemos,et al.  QTL identification for tolerance to fruit set in tomato by fAFLP markers , 2007 .

[157]  Hideyuki Takahashi,et al.  Auxins reverse plant male sterility caused by high temperatures , 2010, Proceedings of the National Academy of Sciences.

[158]  A. Fernie,et al.  Metabolomics-assisted breeding: a viable option for crop improvement? , 2009, Trends in genetics : TIG.

[159]  E. Pacini,et al.  Inter-Conversion of Carbohydrate Reserves from Pollen Maturation to Rehydration in a Chili Pepper , 2013 .

[160]  D. Jackson,et al.  Sugars, signalling, and plant development. , 2012, Journal of experimental botany.

[161]  P. K. Hepler,et al.  POLLEN GERMINATION AND TUBE GROWTH. , 1997, Annual review of plant physiology and plant molecular biology.

[162]  R. Sangwan Change in the amino-acid content during male gametophyte formation of Datura metel in Situ , 1978, Theoretical and Applied Genetics.

[163]  K. Koch,et al.  Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. , 2004, Current opinion in plant biology.

[164]  S. Iwahori,et al.  High temperature injuries in tomato. III. , 1963 .