Sucrose Transporter <i>ZmSut1</i> Expression and Localization Uncover New Insights into Sucrose Phloem Loading

Baker, Robert F.; Leach, Kristen A.; Boyer, Nathanial R.; Swyers, Michael; Benitez‐Alfonso, Yoselin; Skopelitis, Tara; Luo, Anding; Sylvester, Anne W.; Jackson, David; Braun, David

doi:10.1104/pp.16.00884

Cited by 88 publications

(62 citation statements)

References 103 publications

(156 reference statements)

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“…Very recently, Baker et al () demonstrated that ZmSUT1 does not participate in sucrose unloading in sink tissues. At the plant/fungus interface, for example, along the collection or transport phloem, this situation may be different.…”

Section: Discussionmentioning

confidence: 99%

“…Aoki et al () cloned ZmSUT1 complementary DNA (cDNA) from maize and showed that the corresponding gene is expressed in source and sink tissues, such as mature leaf blades and sheaths, as well as pedicels and seeds. Very recently, Baker et al () elucidated the cellular localization pattern of ZmSUT1 transcripts and proteins in more detail. ZmSUT1 is localized both to companion cells, for sucrose loading into the sieve tube system for long‐distance transport, and to phloem and xylem parenchyma cells, as well as to bundle sheath cells, where it functions in sucrose recovery from the apoplasm.…”

Section: Introductionmentioning

confidence: 99%

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The fungal UmSrt1 and maize ZmSUT1 sucrose transporters battle for plant sugar resources

Wittek

Drèyer

Al‐Rasheid

et al. 2017

JIPB

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The biotrophic fungus Ustilago maydis causes corn smut disease, inducing tumor formation in its host Zea mays. Upon infection, the fungal hyphae invaginate the plasma membrane of infected maize cells, establishing an interface where pathogen and host are separated only by their plasma membranes. At this interface the fungal and maize sucrose transporters, UmSrt1 and ZmSUT1, compete for extracellular sucrose in the corn smut/maize pathosystem. Here we biophysically characterized ZmSUT1 and UmSrt1 in Xenopus oocytes with respect to their voltage-, pH-and substrate-dependence and determined affinities toward protons and sucrose. In contrast to ZmSUT1, UmSrt1 has a high affinity for sucrose and is relatively pH-and voltage-independent. Using these quantitative parameters, we developed a mathematical model to simulate the competition for extracellular sucrose at the contact zone between the fungus and the host plant. This approach revealed that UmSrt1 exploits the apoplastic sucrose resource, which forces the plant transporter into a sucrose export mode providing the fungus with sugar from the phloem. Importantly, the high sucrose concentration in the phloem appeared disadvantageous for the ZmSUT1, preventing sucrose recovery from the apoplastic space in the fungus/plant interface.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The fungal UmSrt1 and maize ZmSUT1 sucrose transporters battle for plant sugar resources

Wittek

Drèyer

Al‐Rasheid

et al. 2017

JIPB

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“…New Phytologist efflux from a specific cell type and loading is achieved in a multitier manner. This question is of particular interest because in situ hybridization experiments identified SUT1 in companion cells, xylem and phloem parenchyma, as well as bundle sheath (Baker et al, 2016). With the intent of localizing SWEET13 paralogs, we had generated translational reporter gene fusions that included the first three introns.…”

Section: Researchmentioning

confidence: 99%

“…In monocots, including all cereal crops, the situation is less clear. In maize, the phloem-expressed ZmSUT1 (Baker et al, 2016) (phylogenetically in the SUT2 clade) appears to be critically important for phloem translocation (Slewinski et al, 2009), whereas rice ossut1 mutants and RNAi lines had no apparent growth or yield defects (Ishimaru et al, 2001;Scofield et al, 2002;Eom et al, 2012). As a result, there is an ongoing debate regarding the mechanisms behind phloem loading in cereals (Braun et al, 2014;Regmi et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock‐out mutants in Zea mays

et al. 2018

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SummaryCrop yield depends on efficient allocation of sucrose from leaves to seeds. In Arabidopsis, phloem loading is mediated by a combination of SWEET sucrose effluxers and subsequent uptake by SUT1/SUC2 sucrose/H + symporters. ZmSUT1 is essential for carbon allocation in maize, but the relative contribution to apoplasmic phloem loading and retrieval of sucrose leaking from the translocation path is not known.Here we analysed the contribution of SWEETs to phloem loading in maize.We identified three leaf-expressed SWEET sucrose transporters as key components of apoplasmic phloem loading in Zea mays L. ZmSWEET13 paralogues (a, b, c) are among the most highly expressed genes in the leaf vasculature. Genome-edited triple knock-out mutants were severely stunted. Photosynthesis of mutants was impaired and leaves accumulated high levels of soluble sugars and starch. RNA-seq revealed profound transcriptional deregulation of genes associated with photosynthesis and carbohydrate metabolism. Genome-wide association study (GWAS) analyses may indicate that variability in ZmSWEET13s correlates with agronomical traits, especifically flowering time and leaf angle.This work provides support for cooperation of three ZmSWEET13s with ZmSUT1 in phloem loading in Z. mays.

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“…In monocots, including all cereal crops, the situation is less clear. In maize, the phloem-40 expressed ZmSUT1 (Baker et al, 2016) (phylogenetically in the SUT2 clade) appears to 41 be critically important for phloem translocation (Slewinski et al, 2009), whereas rice 42 ossut1 mutants and RNAi lines had no apparent growth or yield defects (Ishimaru et al, 43 2001;Scofield et al, 2002;Eom et al, 2012). As a result, there is an ongoing debate 44 regarding the mechanisms behind phloem loading in cereals (Braun et al, 2014;Regmi 45 et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Impaired phloem loading in genome-edited triple knock-out mutants of SWEET13 sucrose transporters

Bezrutczyk

Hartwig

Horschman

et al. 2017

Preprint

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One Sentence Summary: Three SWEET sucrose transporter paralogs are necessary for phloem loading in maize.All rights reserved. No reuse allowed without permission.was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint (which . http://dx.doi.org/10.1101/197921 doi: bioRxiv preprint first posted online Oct. 3, 2017; 2 SummaryCrop yield depends on efficient allocation of sucrose from leaves to seeds. In Arabidopsis, phloem loading is mediated by a combination of SWEET sucrose effluxers and subsequent uptake by SUT1/SUC2 sucrose/H + symporters. ZmSUT1 is essential for carbon allocation in maize, but the relative contribution to apoplasmic phloem loading and retrieval of sucrose leaking from the translocation path is not known. We therefor tested whether SWEETs are important for phloem loading in maize.Here we identified three leaf-expressed SWEET sucrose transporters as key This work provides support for cooperation of three ZmSWEET13s with ZmSUT1 in phloem loading in Zea mays L. Our study highlights these three ZmSWEET13 sucrose transporters as possible candidates for the engineering of crop yield.

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Sucrose Transporter ZmSut1 Expression and Localization Uncover New Insights into Sucrose Phloem Loading

Cited by 88 publications

References 103 publications

The fungal UmSrt1 and maize ZmSUT1 sucrose transporters battle for plant sugar resources

The fungal UmSrt1 and maize ZmSUT1 sucrose transporters battle for plant sugar resources

Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock‐out mutants in Zea mays

Impaired phloem loading in genome-edited triple knock-out mutants of SWEET13 sucrose transporters

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