Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity

Claeys, Hannes; Lang, Son; Xu, Xiaosa; Satoh-Nagasawa, Namiko; Eveland, Andrea L.; Goldshmidt, Alexander; Feil, Regina; Beggs, Grace A.; Sakai, Hajime; Brennan, Richard G.; Lunn, John E.; Jackson, David

doi:10.1038/s41477-019-0394-z

Cited by 80 publications

(81 citation statements)

References 39 publications

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“…proteins is uncoupled from their catalytic activities (Claeys et al, 2019), setting a precedent for Tre6P-metabolizing enzymes to have moonlighting functions. Overall, these observations point to OtsA acting as an adequate source of Tre6P when expressed in planta, but lacking some functionalities of TPS1.…”

Section: Role Of Tps1 In the Sucrose-tre6p Nexusmentioning

confidence: 99%

“…TPS2 and TPS4 are not expressed in the right place at the right time in developing seeds to substitute for TPS1, or if the TPS1 protein has unique properties that the other two class I TPS isoforms lack (reviewed in . In this context, it is worth noting that two TPP genes in maize (Zea mays) -RAMOSA3 (RA3) and ZmTPP4 -were recently found to encode catalytically active TPP enzymes that also have non-catalytic functions in regulating inflorescence branching (Satoh-Nagasawa et al, 2006;Claeys et al, 2019), setting a precedent for enzymes in this pathway to have "moonlighting" functions.…”

Section: Introductionmentioning

confidence: 99%

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Functional Features of TREHALOSE-6-PHOSPHATE SYNTHASE1, an Essential Enzyme in Arabidopsis[OPEN]

et al. 2020

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Section: Role Of Tps1 In the Sucrose-tre6p Nexusmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Functional Features of TREHALOSE-6-PHOSPHATE SYNTHASE1, an Essential Enzyme in Arabidopsis[OPEN]

et al. 2020

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“…For 336 example, shoot apical meristem activity in A. thaliana and organogenesis adapt rapidly to 337 changes in nitrate availability in soils through the long-range cytokinin signaling [43]. 338 Inflorescence branching and auxiliary inflorescence meristems fates in maize are regulated by 339 sugar metabolism via the function of three RAMOSA genes [45][46][47][48]. Hormones including 340 auxin and cytokinin have been also known to function in inflorescence architecture with 341 auxin having a critical and conserved role in axillary meristem initiation in A. thaliana and 342 maize [44,49].…”

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YSL3-mediated copper distribution is required for fertility, grain yield, and size inBrachypodium

Sheng

Jiang

Ishka

et al. 2019

Preprint

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35Addressing the looming global food security crisis requires the development of high yielding 36 crops. In this regard, the deficiency for the micronutrient copper in agricultural soils 37 decreases grain yield and significantly impacts a globally important crop, wheat. In cereals, 38 grain yield is determined by inflorescence architecture, flower fertility, grain size and weight. 39 Whether copper is involved in these processes and how it is delivered to the reproductive 40 organs is not well understood. We show that copper deficiency alters not only the grain set 41 but also flower development in both wheat and it's recognized model, Brachypodium 42 distachyon, We then show that a brachypodium yellow-stripe-like 3 (YSL3) transporter 43 localizes to the phloem and mediates copper delivery to flag leaves, anthers and pistils. 44 Failure to deliver copper to these structures in the ysl3 CRISPR/Cas9 mutant results in 45 delayed flowering, altered inflorescence architecture, reduced floret fertility, grain number, 46 size, and weight. These defects are rescued by copper supplementation and are complemented 47 by the YSL3 cDNA. This new knowledge will help to devise sustainable approaches for 48 improving grain yield in regions where soil quality is a major obstacle for crop production. 49 50Global food security and the demand for high-yielding grain crops are among the most urgent 51 drivers of modern plant sciences due to the current trend of population growth, extreme 52 weather conditions and decreasing arable land resources [1]. The grain yield is directly linked 53 to the crop and soil fertility. In this regard, it has been known for decades that the deficiency 54 for the micronutrient copper in alkaline, coarse-textured or organic soils that occupy more 55 than 30% of the world arable land, compromises crop fertility, reduces grain/seed yield and in 56 acute cases results in crop failure [2][3][4][5]. In accord with the essential role of copper in 57 reproduction, recent studies using synchrotron x-ray fluorescent (SXRF) microscopy 58 established that copper localizes to anthers and pistils of flowers in a model dicotyledonous 59 species, Arabidopsis thaliana, and failure to deliver copper to these reproductive organs 60 severely compromises fertility and seed set [6]. Although copper deficiency can be remedied 61 by the application of copper-based fertilizers, this approach is not environmentally friendly 62 and can lead to the build-up of toxic copper levels in soils [2,5,7]. Mineral nutrient 63 transporters have been recognized as key targets for improving the mineral use efficiency in 64 sustainable crop production [8]. Wheat is the world's third important staple crop after maize 65 (Zea mays) and rice (Oryza sativa); however, wheat grain yield remained relatively low under 66 marginal growing environments despite significant breeding efforts [9]. Wheat is also 67 regarded as the most sensitive to copper deficiency [2, 3,5]. How copper uptake and internal 68 transport is achieved in wheat and how it af...

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“…RAMOSA3 controls inflorescence architecture in maize and was found to be encoded by a TPP gene which regulates meristem fate through catalytically inactive TPPs also including TPP4 [30,31]. No effect of these TPPs on T6P has been proven and a moonlighting role for TPP4 has been put forward; the exact mechanism through which meristem fate is regulated by TPPs is not known.…”

Section: Maizementioning

confidence: 99%

Trehalose 6-phosphate signalling and impact on crop yield

Paul

Watson

Griffiths

2020

Biochemical Society Transactions

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The domestication and breeding of crops has been a major achievement for mankind enabling the development of stable societies and civilisation. Crops have become more productive per unit area of cultivated land over the course of domestication supporting a current global population of 7.8 billion. Food security crops such as wheat and maize have seen large changes compared with early progenitors. Amongst processes that have been altered in these crops, is the allocation of carbon resources to support larger grain yield (grain number and size). In wheat, reduction in stem height has enabled diversion of resources from stems to ears. This has freed up carbon to support greater grain yield. Green revolution genes responsible for reductions in stem height are known, but a unifying mechanism for the active regulation of carbon resource allocation towards and within sinks has however been lacking. The trehalose 6-phosphate (T6P) signalling system has emerged as a mechanism of resource allocation and has been implicated in several crop traits including assimilate partitioning and improvement of yield in different environments. Understanding the mode of action of T6P through the SnRK1 protein kinase regulatory system is providing a basis for a unifying mechanism controlling whole-plant resource allocation and source-sink interactions in crops. Latest results show it is likely that the T6P/SnRK1 pathway can be harnessed for further improvements such as grain number and grain filling traits and abiotic stress resilience through targeted gene editing, breeding and chemical approaches.

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Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity

Cited by 80 publications

References 39 publications

Functional Features of TREHALOSE-6-PHOSPHATE SYNTHASE1, an Essential Enzyme in Arabidopsis[OPEN]

Functional Features of TREHALOSE-6-PHOSPHATE SYNTHASE1, an Essential Enzyme in Arabidopsis[OPEN]

YSL3-mediated copper distribution is required for fertility, grain yield, and size inBrachypodium

Trehalose 6-phosphate signalling and impact on crop yield

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