skip to main content

Title: Sugar flux and signaling in plant–microbe interactions

Plant breeders have developed crop plants that are resistant to pests, but the continual evolution of pathogens creates the need to iteratively develop new control strategies. Molecular tools have allowed us to gain deep insights into disease responses, allowing for more efficient, rational engineering of crops that are more robust or resistant to a greater number of pathogen variants. Here we describe the roles ofSWEETandSTPtransporters, membrane proteins that mediate transport of sugars across the plasma membrane. We discuss how these transporters may enhance or restrict disease through controlling the level of nutrients provided to pathogens and whether the transporters play a role in sugar signaling for disease resistance. This review indicates open questions that require further research and proposes the use of genome editing technologies for engineering disease resistance.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
The Plant Journal
Page Range / eLocation ID:
p. 675-685
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    Cultivated cotton (Gossypium hirsutum) is the most important fibre crop in the world. Cotton leaf curl disease (CLCuD) is the major limiting factor and a threat to textile industry in India and Pakistan. All the local cotton cultivars exhibit moderate to no resistance againstCLCuD. In this study, we evaluated an exotic cotton accession Mac7 as a resistance source toCLCuD by challenging it with viruliferous whiteflies and performingqPCRto evaluate the presence/absence and relative titre ofCLCuD‐associated geminiviruses/betasatellites. The results indicated that replication of pathogenicity determinant betasatellite is significantly attenuated in Mac7 and probably responsible for resistance phenotype. Afterwards, to decipher the genetic basis ofCLCuD resistance in Mac7, we performedRNAsequencing onCLCuD‐infested Mac7 and validatedRNA‐Seq data withqPCRon 24 independent genes. We performed co‐expression network and pathway analysis for regulation of geminivirus/betasatellite‐interacting genes. We identified nine novel modules with 52 hubs of highly connected genes in network topology within the co‐expression network. Analysis of these hubs indicated the differential regulation of auxin stimulus and cellular localization pathways in response toCLCuD. We also analysed the differential regulation of geminivirus/betasatellite‐interacting genes in Mac7. We further performed the functional validation of selected candidate genes via virus‐induced gene silencing (VIGS). Finally, we evaluated the genomic context of resistance responsive genes and found that these genes are not specific to A or D sub‐genomes ofG. hirsutum. These results have important implications in understandingCLCuD resistance mechanism and developing a durable resistance in cultivated cotton.

    more » « less
  2. Summary

    One of the most fascinating and exciting periods in my scientific career entailed dissecting the symbiotic relationship between two membrane transporters, the Nicotinamide adenine dinucleotide phosphate reduced form (NADPH) oxidase complex and voltage‐gated proton channels (HV1). By the time I entered this field, there had already been substantial progress toward understandingNADPHoxidase, but HV1 were known only to a tiny handful of cognoscenti around the world. Having identified the first proton currents in mammalian cells in 1991, I needed to find a clear function for these molecules if the work was to become fundable. The then‐recent discoveries of Henderson, Chappell, and colleagues in 1987–1988 that led them to hypothesize interactions of both molecules during the respiratory burst of phagocytes provided an excellent opportunity. In a nutshell, both transporters function by moving electrical charge across the membrane:NADPHoxidase moves electrons and HV1 moves protons. The consequences of electrogenicNADPHoxidase activity on both membrane potential and pH strongly self‐limit this enzyme. Fortunately, both consequences specifically activate HV1, and HV1 activity counteracts both consequences, a kind of yin–yang relationship. Notwithstanding a decade starting in 1995 when many believed the opposite, these are two separate molecules that function independently despite their being functionally interdependent in phagocytes. The relationship betweenNADPHoxidase and HV1 has become a paradigm that somewhat surprisingly has now extended well beyond the phagocyteNADPHoxidase – an industrial strength producer of reactive oxygen species (ROS) – to myriad other cells that produce orders of magnitude lessROSfor signaling purposes. These cells with their sevenNADPHoxidase (NOX) isoforms provide a vast realm of mechanistic obscurity that will occupy future studies for years to come.

    more » « less
  3. Summary

    In flowering plants, cell–cell communication plays a key role in reproductive success, as both pollination and fertilization require pathways that regulate interactions between many different cell types. Some of the most critical of these interactions are those between the pollen tube (PT) and the embryo sac, which ensure the delivery of sperm cells required for double fertilization. Synergid cells function to attract thePTthrough secretion of small peptides and inPTreception via membrane‐bound proteins associated with the endomembrane system and the cell surface. While many synergid‐expressed components regulatingPTattraction and reception have been identified, few tools exist to study the localization of membrane‐bound proteins and the components of the endomembrane system in this cell type. In this study, we describe the localization and distribution of seven fluorescent markers that labelled components of the secretory pathway in synergid cells ofArabidopsis thaliana. These markers were used in co‐localization experiments to investigate the subcellular distribution of the twoPTreception componentsLORELEI, aGPI‐anchored surface protein, andNORTIA, aMILDEW RESISTANCE LOCUSO protein, both found within the endomembrane system of the synergid cell. These secretory markers are useful tools for both reproductive and cell biologists, enabling the analysis of membrane‐associated trafficking within a haploid cell actively involved in polar transport.

    more » « less
  4. Abstract

    Desiccation resistance, the ability of an organism to reduce water loss, is an essential trait in arid habitats. Drought frequency in tropical regions is predicted to increase with climate change, and small ectotherms are often under a strong desiccation risk. We tested hypotheses regarding the underexplored desiccation potential of tropical insects. We measured desiccation resistance in 82 ant species from a Panama rainforest by recording the time ants can survive desiccation stress. Species' desiccation resistance ranged from 0.7 h to 97.9 h. We tested the desiccation adaptation hypothesis, which predicts higher desiccation resistance in habitats with higher vapor pressure deficit (VPD) – the drying power of the air. In a Panama rainforest, canopy microclimates averaged aVPDof 0.43kPa, compared to aVPDof 0.05kPa in the understory. Canopy ants averaged desiccation resistances 2.8 times higher than the understory ants. We tested a number of mechanisms to account for desiccation resistance. Smaller insects should desiccate faster given their higher surface area to volume ratio. Desiccation resistance increased with ant mass, and canopy ants averaged 16% heavier than the understory ants. A second way to increase desiccation resistance is to carry more water. Water content was on average 2.5% higher in canopy ants, but total water content was not a good predictor of ant desiccation resistance or critical thermal maximum (CTmax), a measure of an ant's thermal tolerance. In canopy ants, desiccation resistance andCTmaxwere inversely related, suggesting a tradeoff, while the two were positively correlated in understory ants. This is the first community level test of desiccation adaptation hypothesis in tropical insects. Tropical forests do contain desiccation‐resistant species, and while we cannot predict those simply based on their body size, high levels of desiccation resistance are always associated with the tropical canopy.

    more » « less
  5. Summary

    We investigated the molecular basis and physiological implications of anion transport during pollen tube (PT) growth inArabidopsis thaliana(Col‐0).

    Patch‐clamp whole‐cell configuration analysis of pollen grain protoplasts revealed three subpopulations of anionic currents differentially regulated by cytoplasmic calcium ([Ca2+]cyt). We investigated the pollen‐expressed proteinsAtSLAH3,AtALMT12,AtTMEM16 andAtCCCas the putative anion transporters responsible for these currents.

    AtCCCGFPwas observed at the shank andAtSLAH3‐GFPat the tip and shank of thePTplasma membrane. Both are likely to carry the majority of anion current at negative potentials, as extracellular anionic fluxes measured at the tip ofPTs with an anion vibrating probe were significantly lower inslah3−/−andccc−/−mutants, but unaffected inalmt12−/−andtmem16−/−. We further characterised the effect ofpHandGABAby patch clamp. Strong regulation by extracellularpHwas observed in the wild‐type, but not intmem16−/−. Our results are compatible withAtTMEM16 functioning as an anion/H+cotransporter and therefore, as a putativepHsensor.GABApresence: (1) inhibited the overall currents, an effect that is abrogated in thealmt12−/−and (2) reduced the current inAtALMT12 transfectedCOS‐7 cells, strongly suggesting the direct interaction ofGABAwithAtALMT12.

    Our data show thatAtSLAH3 andAtCCCactivity is sufficient to explain the major component of extracellular anion fluxes, and unveils a possible regulatory system linkingPTgrowth modulation bypH,GABA, and [Ca2+]cytthrough anionic transporters.

    more » « less