Increasing Amyloplast Size in Wheat Endosperm Through Mutation of PARC6 Affects Starch Granule Morphology

Overview

Journal New Phytol

Specialty Biology

Date 2023 Jul 10

PMID 37424336

Authors

Lara Esch

Qi Yang Ngai

J Elaine Barclay

Rose McNelly

Sadiye Hayta

Mark A Smedley

Alison M Smith

David Seung

Affiliations

Soon will be listed here.

Abstract

The determination of starch granule morphology in plants is poorly understood. The amyloplasts of wheat endosperm contain large discoid A-type granules and small spherical B-type granules. To study the influence of amyloplast structure on these distinct morphological types, we isolated a mutant in durum wheat (Triticum turgidum) defective in the plastid division protein PARC6, which had giant plastids in both leaves and endosperm. Endosperm amyloplasts of the mutant contained more A- and B-type granules than those of the wild-type. The mutant had increased A- and B-type granule size in mature grains, and its A-type granules had a highly aberrant, lobed surface. This morphological defect was already evident at early stages of grain development and occurred without alterations in polymer structure and composition. Plant growth and grain size, number and starch content were not affected in the mutants despite the large plastid size. Interestingly, mutation of the PARC6 paralog, ARC6, did not increase plastid or starch granule size. We suggest TtPARC6 can complement disrupted TtARC6 function by interacting with PDV2, the outer plastid envelope protein that typically interacts with ARC6 to promote plastid division. We therefore reveal an important role of amyloplast structure in starch granule morphogenesis in wheat.

Citing Articles

Distinct effects of PTST2b and MRC on starch granule morphogenesis in potato tubers.

Hochmuth A, Carswell M, Rowland A, Scarbrough D, Esch L, Kamble N Plant Biotechnol J. 2024; 23(2):412-429.

PMID: 39659019 PMC: 11772324. DOI: 10.1111/pbi.14505.

Wheat MYOSIN-RESEMBLING CHLOROPLAST PROTEIN controls B-type starch granule initiation timing during endosperm development.

Chen J, Chen Y, Watson-Lazowski A, Hawkins E, Barclay J, Fahy B Plant Physiol. 2024; 196(3):1980-1996.

PMID: 39158075 PMC: 11531834. DOI: 10.1093/plphys/kiae429.

High-yield hybrid breeding of Camellia oleifolia based on ISSR molecular markers.

Zheng J, Su H, Pu S, Chen H, El-Kassaby Y, Yang Z BMC Plant Biol. 2024; 24(1):517.

PMID: 38851667 PMC: 11162053. DOI: 10.1186/s12870-024-05218-x.

Principles of amyloplast replication in the ovule integuments of Arabidopsis thaliana.

Fujiwara M, Yoshioka Y, Kazama Y, Hirano T, Niwa Y, Moriyama T Plant Physiol. 2024; 196(1):137-152.

PMID: 38829834 PMC: 11376375. DOI: 10.1093/plphys/kiae314.

SAGA1 and SAGA2 promote starch formation around proto-pyrenoids in Arabidopsis chloroplasts.

Atkinson N, Stringer R, Mitchell S, Seung D, McCormick A Proc Natl Acad Sci U S A. 2024; 121(4):e2311013121.

PMID: 38241434 PMC: 10823261. DOI: 10.1073/pnas.2311013121.

References

Osteryoung K, Pyke K . Division and dynamic morphology of plastids. Annu Rev Plant Biol. 2014; 65:443-72. DOI: 10.1146/annurev-arplant-050213-035748. View

Miyagishima S . Mechanism of plastid division: from a bacterium to an organelle. Plant Physiol. 2011; 155(4):1533-44. PMC: 3091088. DOI: 10.1104/pp.110.170688. View

Marbouty M, Saguez C, Cassier-Chauvat C, Chauvat F . ZipN, an FtsA-like orchestrator of divisome assembly in the model cyanobacterium Synechocystis PCC6803. Mol Microbiol. 2009; 74(2):409-20. DOI: 10.1111/j.1365-2958.2009.06873.x. View

Vitha S, Froehlich J, Koksharova O, Pyke K, van Erp H, Osteryoung K . ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell. 2003; 15(8):1918-33. PMC: 167179. DOI: 10.1105/tpc.013292. View

Yun M, Kawagoe Y . Septum formation in amyloplasts produces compound granules in the rice endosperm and is regulated by plastid division proteins. Plant Cell Physiol. 2010; 51(9):1469-79. DOI: 10.1093/pcp/pcq116. View

Howard T, Rejab N, Griffiths S, Leigh F, Leverington-Waite M, Simmonds J . Identification of a major QTL controlling the content of B-type starch granules in Aegilops. J Exp Bot. 2011; 62(6):2217-28. PMC: 3060699. DOI: 10.1093/jxb/erq423. View

Cai Y, Chen H, Xiao N, Wu Y, Yu L, Chen Z . Substandard starch grain4 may function in amyloplast development by influencing starch and lipid metabolism in rice endosperm. J Plant Physiol. 2022; 270:153638. DOI: 10.1016/j.jplph.2022.153638. View

Zhang M, Hu Y, Jia J, Li D, Zhang R, Gao H . CDP1, a novel component of chloroplast division site positioning system in Arabidopsis. Cell Res. 2009; 19(7):877-86. DOI: 10.1038/cr.2009.78. View

Fahy B, Gonzalez O, Savva G, Ahn-Jarvis J, Warren F, Dunn J . Loss of starch synthase IIIa changes starch molecular structure and granule morphology in grains of hexaploid bread wheat. Sci Rep. 2022; 12(1):10806. PMC: 9233681. DOI: 10.1038/s41598-022-14995-0. View

10.

Chen J, Hawkins E, Seung D . Towards targeted starch modification in plants. Curr Opin Plant Biol. 2021; 60:102013. DOI: 10.1016/j.pbi.2021.102013. View

11.

Streb S, Delatte T, Umhang M, Eicke S, Schorderet M, Reinhardt D . Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell. 2008; 20(12):3448-66. PMC: 2630441. DOI: 10.1105/tpc.108.063487. View

12.

Langeveld S, van Wijk R, Stuurman N, Kijne J, de Pater S . B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression. J Exp Bot. 2000; 51(349):1357-61. View

13.

Zhang M, Chen C, Froehlich J, TerBush A, Osteryoung K . Roles of Arabidopsis PARC6 in Coordination of the Chloroplast Division Complex and Negative Regulation of FtsZ Assembly. Plant Physiol. 2015; 170(1):250-62. PMC: 4704591. DOI: 10.1104/pp.15.01460. View

14.

Koksharova O, Wolk C . A novel gene that bears a DnaJ motif influences cyanobacterial cell division. J Bacteriol. 2002; 184(19):5524-8. PMC: 135336. DOI: 10.1128/JB.184.19.5524-5528.2002. View

15.

Sun T, Yuan H, Cao H, Yazdani M, Tadmor Y, Li L . Carotenoid Metabolism in Plants: The Role of Plastids. Mol Plant. 2017; 11(1):58-74. DOI: 10.1016/j.molp.2017.09.010. View

16.

Ishikawa H, Yasuzawa M, Koike N, Sanjaya A, Moriyama S, Nishizawa A . PARC6 Is Critical for Plastid Morphogenesis in Pavement, Trichome, and Guard Cells in Leaf Epidermis. Front Plant Sci. 2020; 10:1665. PMC: 6974557. DOI: 10.3389/fpls.2019.01665. View

17.

Chia T, Chirico M, King R, Ramirez-Gonzalez R, Saccomanno B, Seung D . A carbohydrate-binding protein, B-GRANULE CONTENT 1, influences starch granule size distribution in a dose-dependent manner in polyploid wheat. J Exp Bot. 2019; 71(1):105-115. DOI: 10.1093/jxb/erz405. View

18.

Yun M, Kawagoe Y . Amyloplast division progresses simultaneously at multiple sites in the endosperm of rice. Plant Cell Physiol. 2009; 50(9):1617-26. DOI: 10.1093/pcp/pcp104. View

19.

Mazouni K, Domain F, Cassier-Chauvat C, Chauvat F . Molecular analysis of the key cytokinetic components of cyanobacteria: FtsZ, ZipN and MinCDE. Mol Microbiol. 2004; 52(4):1145-58. DOI: 10.1111/j.1365-2958.2004.04042.x. View

20.

Matsushima R, Maekawa M, Kusano M, Kondo H, Fujita N, Kawagoe Y . Amyloplast-localized SUBSTANDARD STARCH GRAIN4 protein influences the size of starch grains in rice endosperm. Plant Physiol. 2013; 164(2):623-36. PMC: 3912094. DOI: 10.1104/pp.113.229591. View