Induction of male sterility in plants by metabolic engineering of the carbohydrate supply

Goetz, Marc; Godt, Dietmute E.; Guivarc’h, Anne; Kahmann, Uwe; Chriqui, Dominique; Roitsch, Thomas

doi:10.1073/pnas.091097998

Cited by 298 publications

(266 citation statements)

References 55 publications

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“…Drought-induced carbohydrate deprivation, enhanced endogenous abscisic acid concentration, and an impaired ability to utilize the incoming sucrose by the reproductive sinks are potential factors contributing to seed abortion in grain crops (Setter et al, 2001). A reduced acid invertase activity can arrest the development of reproductive tissues due to improper phloem unloading (Goetz et al, 2001). In addition, drought stress may inhibit important functions of vacuolar invertasemediated sucrose hydrolysis and osmotic potential modulation.…”

Section: Assimilate Partitioningmentioning

confidence: 99%

Plant drought stress: effects, mechanisms and management

Farooq

Wahid

Kobayashi

et al. 2009

Agron. Sustain. Dev.

2,830

1,622

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-Scarcity of water is a severe environmental constraint to plant productivity. Drought-induced loss in crop yield probably exceeds losses from all other causes, since both the severity and duration of the stress are critical. Here, we have reviewed the effects of drought stress on the growth, phenology, water and nutrient relations, photosynthesis, assimilate partitioning, and respiration in plants. This article also describes the mechanism of drought resistance in plants on a morphological, physiological and molecular basis. Various management strategies have been proposed to cope with drought stress. Drought stress reduces leaf size, stem extension and root proliferation, disturbs plant water relations and reduces water-use efficiency. Plants display a variety of physiological and biochemical responses at cellular and whole-organism levels towards prevailing drought stress, thus making it a complex phenomenon. CO 2 assimilation by leaves is reduced mainly by stomatal closure, membrane damage and disturbed activity of various enzymes, especially those of CO 2 fixation and adenosine triphosphate synthesis. Enhanced metabolite flux through the photorespiratory pathway increases the oxidative load on the tissues as both processes generate reactive oxygen species. Injury caused by reactive oxygen species to biological macromolecules under drought stress is among the major deterrents to growth. Plants display a range of mechanisms to withstand drought stress. The major mechanisms include curtailed water loss by increased diffusive resistance, enhanced water uptake with prolific and deep root systems and its efficient use, and smaller and succulent leaves to reduce the transpirational loss. Among the nutrients, potassium ions help in osmotic adjustment; silicon increases root endodermal silicification and improves the cell water balance. Low-molecular-weight osmolytes, including glycinebetaine, proline and other amino acids, organic acids, and polyols, are crucial to sustain cellular functions under drought. Plant growth substances such as salicylic acid, auxins, gibberrellins, cytokinin and abscisic acid modulate the plant responses towards drought. Polyamines, citrulline and several enzymes act as antioxidants and reduce the adverse effects of water deficit. At molecular levels several drought-responsive genes and transcription factors have been identified, such as the dehydration-responsive element-binding gene, aquaporin, late embryogenesis abundant proteins and dehydrins. Plant drought tolerance can be managed by adopting strategies such as mass screening and breeding, marker-assisted selection and exogenous application of hormones and osmoprotectants to seed or growing plants, as well as engineering for drought resistance. drought response / stomatal oscillation / osmoprotectants / hormones / stress proteins / drought management / CO 2

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Section: Assimilate Partitioningmentioning

confidence: 99%

Plant drought stress: effects, mechanisms and management

Farooq

Wahid

Kobayashi

et al. 2009

Agron. Sustain. Dev.

2,830

1,622

View full text Add to dashboard Cite

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“…5) showed only the hexoses, Glc and Fru, and no detectable Suc in any of our samples. In tobacco, Goetz et al (2001) have shown a critical role of cell wall invertase in tapetal cells before their degeneration. Thus, it is possible that, as in tobacco, hexose sugars are the main source of carbon that is transported into the developing maize pollen.…”

Section: Sugar Profiles Metabolic Sensing and Gene Expressionmentioning

confidence: 99%

Starch Biosynthesis during Pollen Maturation Is Associated with Altered Patterns of Gene Expression in Maize

2002

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Starch biosynthesis during pollen maturation is not well understood in terms of genes/proteins and intracellular controls that regulate it in developing pollen. We have studied two specific developmental stages: "early," characterized by the lack of starch, before or during pollen mitosis I; and "late," an actively starch-filling post-pollen mitosis I phase in S-type cytoplasmic male-sterile (S-CMS) and two related male-fertile genotypes. The male-fertile starch-positive, but not the CMS starch-deficient, genotypes showed changes in the expression patterns of a large number of genes during this metabolic transition. In addition to a battery of housekeeping genes of carbohydrate metabolism, we observed changes in hexose transporter, plasma membrane H ϩ -ATPase, ZmMADS1, and 14-3-3 proteins. Reduction or deficiency in 14-3-3 protein levels in all three major cellular sites (amyloplasts [starch], mitochondria, and cytosol) in male-sterile relative to male-fertile genotypes are of potential interest because of interorganellar communication in this CMS system. Further, the levels of hexose sugars were significantly reduced in male-sterile as compared with male-fertile tissues, not only at "early" and "late" stages but also at an earlier point during meiosis. Collectively, these data suggest that combined effects of both reduced sugars and their reduced flux in starch biosynthesis along with a strong possibility for altered redox passage may lead to the observed temporal changes in gene expressions, and ultimately pollen sterility.Several excellent reviews on male gametophyte development in plants (Mascarenhas, 1989; Bewley et al., 2000) and maize (Zea mays) in particular (Bedinger, 1992;McCormick, 1993) have been written recently and provide overviews of events from meiosis to mature pollen development. In brief, haploid gametes as tetrads are encased in a callose wall and are well nourished through the sporophytic cell layer, tapetum. The role of the tapetum in pollen development is recently elaborated (Liu et al., 2001). Release of single, free microspores from each tetrad is achieved by callase secreted from the tapetal cells, which degenerate and lead to the symplastic isolation of microspores from the mother plant. All nourishments for developing microspores are transported presumably from the nutrient-rich locular fluid inside the anthers. Most importantly, symplastic discontinuity requires that the individual microspores be programmed with appropriate signals or at least be activated for major functions, including the two mitotic divisions, intracellular vacuolar biogenesis, and several metabolic changes such as starch biosynthesis.Starch biosynthesis during the final phases of pollen maturation is critical not only because starch is a reserve source of energy for pollen germination but it also serves as a checkpoint of pollen maturity. Very often, pollen maturation appears to be prematurely terminated if starch levels remain lower than a certain threshold point as evident from several genetically controlled...

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“…In petunia pollen during in vitro germination, a high invertase-like activity was measured, and in a germination medium which contained sucrose as the only carbon source, only the sugars glucose and fructose were detected after 13 h of germination (Ylstra et al 1998). Wall-bound invertase activity was reported earlier to be present on lily pollen (Singh and Knox 1984), and more recently, other plants have been found to express genes or enzyme activity for soluble invertases in floral tissues, particularly in anthers and pollen (Miller and Ranwala 1994, Davies and Robinson 1996, Weber et al 1996, Xu et al 1996, Maddison et al 1999, Goetz et al 2001. The fact that pollen exhibits such invertase activity strongly suggests that pollen imports carbohydrates in the form of monosaccharides, and it was shown that the antisense repression of a tapetum-and pollen-specific extracellular invertase Nin88 in tobacco induced male sterility (Goetz et al 2001).…”

Section: Discussionmentioning

confidence: 99%

Promoter activity of a putative pollen monosaccharide transporter in Petunia hybrida and characterisation of a transposon insertion mutant

2006

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Summary.For the growth of the male reproductive cells of plants, the pollen, the presence of sufficient sucrose or monosaccharides is of vital importance. From Petunia hybrida a pollen-specific putative monosaccharide transporter designated PMT1 (for petunia monosaccharide transporter) has been identified previously. The present work provides an in-depth analysis and characterisation of PMT1 in the context of pollen development with the GUS reporter gene and an insertion mutant. The promoter of the pollen-specific putative PMT1 gene has been isolated by inverse PCR and sequenced. Analysis of plants transformed with the promoter-GUS fusion confirmed the specificity of this gene, belonging to the late pollen-specific expressed genes. GUS activity was detected even after 24 h of in vitro pollen germination, at the pollen tube tip. To elucidate the importance of PMT1 for gametophyte development and fertilisation, we isolated a mutant plant containing a transposon insertion in the PMT1 gene by the dTph1 transposon-tagging PCR-based assay. The PMT1 mutant contained a dTph1 insertion in position 1474 bp of the transcribing part of the gene, before the last two transmembrane-spanning domains. Analysis of the progeny of the heterozygous mutant after selfing revealed no alterations in pollen viability and fertility. Mature pollen grains of a plant homozygous for the transposon insertion were able to germinate in vitro in a medium containing sucrose, glucose, or fructose, which indicates that PMT1 is not essential for pollen survival. Several explanations for these results are discussed in the present work.

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Induction of male sterility in plants by metabolic engineering of the carbohydrate supply

Cited by 298 publications

References 55 publications

Plant drought stress: effects, mechanisms and management

Plant drought stress: effects, mechanisms and management

Starch Biosynthesis during Pollen Maturation Is Associated with Altered Patterns of Gene Expression in Maize

Promoter activity of a putative pollen monosaccharide transporter in Petunia hybrida and characterisation of a transposon insertion mutant

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