The Rice BZ1 Locus Is Required for Glycosylation of Arabinogalactan Proteins and Galactolipid and Plays a Role in both Mechanical Strength and Leaf Color.

AGPs Cell wall Chloroplast Leaf color MGDG Mechanical strength UDP-galactose/glucose epimerase

Journal

Rice (New York, N.Y.)
ISSN: 1939-8425
Titre abrégé: Rice (N Y)
Pays: United States
ID NLM: 101503136

Informations de publication

Date de publication:
17 Jun 2020
Historique:
received: 05 01 2020
accepted: 11 06 2020
entrez: 20 6 2020
pubmed: 20 6 2020
medline: 20 6 2020
Statut: epublish

Résumé

The cell wall and chloroplast are two fundamental structures determining plant mechanical strength and grain yield. Therefore, understanding mechanisms that improve plants' ability to develop a robust cell wall and well-developed chloroplast is of utmost importance for agricultural activities. In this study, we report the functional characterization of a novel rice mutant, brittle stem and zebra leaf (bz1), which displays altered cell wall composition and collapsed chloroplast membrane. Molecular and biochemical analysis revealed that BZ1 encodes a functional UDP-galactose/glucose epimerase (UGE) and is ubiquitously expressed with higher expression in stem and leaf tissues. Multiple techniques analyses, including immunoblots, immuno-gold, and cryogenic scanning electron microscopy, demonstrated a significantly impaired glycosylation of arabinogalactan proteins (AGPs) and disordered cellulose microfibril deposition in bz1. Lipid profiling assay showed that the amount of monogalactosyldiacylglycerols (MGDG), a major chloroplast membrane glycolipid, was significantly decreased in bz1. Taken together, these results strongly demonstrate that BZ1 participates in UDP-galactose supply for the sugar chains biosynthesis of AGPs and MGDG, which thereby, respectively, results in altered cell wall and abnormal chloroplast development. Due to inferior mechanical strength and reduced photosynthesis, bz1 plants displayed detrimental agronomic traits, whereas BZ1 overexpressing lines showed enhanced plant growth. Transcriptome analysis of stems and leaves further showed that numerous key genes involved in AGPs biosynthesis and photosynthesis metabolism were substantially suppressed in bz1. Our finding identifies BZ1 as a dual-targeting UGE protein for glycosylation of AGPs and MGDG and suggests a strategy for breeding robust elite crops.

Sections du résumé

BACKGROUND BACKGROUND
The cell wall and chloroplast are two fundamental structures determining plant mechanical strength and grain yield. Therefore, understanding mechanisms that improve plants' ability to develop a robust cell wall and well-developed chloroplast is of utmost importance for agricultural activities.
RESULTS RESULTS
In this study, we report the functional characterization of a novel rice mutant, brittle stem and zebra leaf (bz1), which displays altered cell wall composition and collapsed chloroplast membrane. Molecular and biochemical analysis revealed that BZ1 encodes a functional UDP-galactose/glucose epimerase (UGE) and is ubiquitously expressed with higher expression in stem and leaf tissues. Multiple techniques analyses, including immunoblots, immuno-gold, and cryogenic scanning electron microscopy, demonstrated a significantly impaired glycosylation of arabinogalactan proteins (AGPs) and disordered cellulose microfibril deposition in bz1. Lipid profiling assay showed that the amount of monogalactosyldiacylglycerols (MGDG), a major chloroplast membrane glycolipid, was significantly decreased in bz1. Taken together, these results strongly demonstrate that BZ1 participates in UDP-galactose supply for the sugar chains biosynthesis of AGPs and MGDG, which thereby, respectively, results in altered cell wall and abnormal chloroplast development. Due to inferior mechanical strength and reduced photosynthesis, bz1 plants displayed detrimental agronomic traits, whereas BZ1 overexpressing lines showed enhanced plant growth. Transcriptome analysis of stems and leaves further showed that numerous key genes involved in AGPs biosynthesis and photosynthesis metabolism were substantially suppressed in bz1.
CONCLUSIONS CONCLUSIONS
Our finding identifies BZ1 as a dual-targeting UGE protein for glycosylation of AGPs and MGDG and suggests a strategy for breeding robust elite crops.

Identifiants

pubmed: 32556633
doi: 10.1186/s12284-020-00400-9
pii: 10.1186/s12284-020-00400-9
pmc: PMC7300173
doi:

Types de publication

Journal Article

Langues

eng

Pagination

41

Références

Curr Biol. 2002 Oct 29;12(21):1840-5
pubmed: 12419184
Annu Rev Plant Biol. 2010;61:263-89
pubmed: 20192742
Curr Opin Plant Biol. 2010 Jun;13(3):305-12
pubmed: 20097119
J Integr Plant Biol. 2011 Feb;53(2):136-42
pubmed: 21205179
Plant Biotechnol J. 2015 May;13(4):514-25
pubmed: 25418842
Plant Cell. 2007 May;19(5):1565-79
pubmed: 17496119
Plant J. 2013 Dec;76(6):1016-29
pubmed: 24128328
J Biol Chem. 2004 Oct 29;279(44):45503-11
pubmed: 15322080
Plant Biotechnol J. 2017 Sep;15(9):1093-1104
pubmed: 28117552
Plant Physiol. 2013 Mar;161(3):1278-90
pubmed: 23349362
Curr Biol. 2017 Sep 11;27(17):R865-R870
pubmed: 28898654
J Biol Chem. 1990 Jan 25;265(3):1319-26
pubmed: 2153126
Anal Biochem. 1985 Aug 1;148(2):446-50
pubmed: 3933380
Annu Rev Cell Dev Biol. 2006;22:53-78
pubmed: 16824006
Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):8175-9
pubmed: 10869420
Plant Physiol. 2010 Jun;153(2):403-19
pubmed: 20388666
J Biol Chem. 2006 Jun 23;281(25):17276-85
pubmed: 16644739
Plant Mol Biol. 2005 Feb;57(3):333-42
pubmed: 15830125
Plant Physiol. 2008 Sep;148(1):580-92
pubmed: 18641085
New Phytol. 2019 Jul;223(2):565-574
pubmed: 30721547
Plant J. 2010 Jul;63(2):312-28
pubmed: 20444225
Nat Rev Mol Cell Biol. 2005 Nov;6(11):850-61
pubmed: 16261190
Plant Cell. 1993 Jan;5(1):9-23
pubmed: 8439747
Curr Opin Plant Biol. 2006 Jun;9(3):248-55
pubmed: 16603411
Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10960-5
pubmed: 11553816
Plant Physiol. 2013 Apr;161(4):1615-33
pubmed: 23391577
BMC Plant Biol. 2014 Nov 18;14:299
pubmed: 25407280
Carbohydr Res. 2015 Sep 23;414:8-14
pubmed: 26162744
Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):17216-21
pubmed: 17940034
Eur J Biochem. 1999 Nov;265(3):990-1001
pubmed: 10518794
PLoS Pathog. 2017 Nov 13;13(11):e1006724
pubmed: 29131851
Biotechnol Biofuels. 2018 Nov 1;11:298
pubmed: 30410573
Science. 2006 Mar 31;311(5769):1940-2
pubmed: 16574868
Mol Plant. 2018 Jan 8;11(1):75-94
pubmed: 29054565
Plant Cell. 2004 Mar;16(3):723-30
pubmed: 14973160
PLoS Genet. 2011 Jul;7(7):e1002196
pubmed: 21829379
Anal Biochem. 1969 Dec;32(3):420-4
pubmed: 5361396
New Phytol. 2015 Jun;206(4):1314-27
pubmed: 25676073
Biochem J. 2006 Feb 15;394(Pt 1):115-24
pubmed: 16266295
Biochem J. 1962 Nov;85:383-8
pubmed: 14002491
Plant Physiol. 2010 Jun;153(2):485-513
pubmed: 20395450
Photosynth Res. 1986 Jan;9(1-2):239-49
pubmed: 24442300
J Biol Chem. 2002 Aug 30;277(35):31994-2002
pubmed: 12077151
Planta. 2010 Jun;232(1):95-108
pubmed: 20369251
Plant Cell Physiol. 2009 Nov;50(11):1886-97
pubmed: 19812064
Science. 2016 Jul 8;353(6295):166-9
pubmed: 27387950
J Nutr. 1998 Feb;128(2):239-45
pubmed: 9446850
Science. 2004 Dec 24;306(5705):2206-11
pubmed: 15618507
Plant J. 2010 May 1;62(4):689-703
pubmed: 20202165
Bioresour Technol. 2013 Feb;130:30-7
pubmed: 23298647
Annu Rev Plant Biol. 2014;65:69-94
pubmed: 24579997
Plant J. 2002 Oct;32(1):105-13
pubmed: 12366804
Am J Bot. 2008 Dec;95(12):1491-7
pubmed: 21628156
Plant Physiol. 1949 Jan;24(1):1-15
pubmed: 16654194

Auteurs

Sitong Liu (S)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China.

Yijun Tang (Y)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China.

Nan Ruan (N)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China.

Zhengjun Dang (Z)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China.

Yuwei Huang (Y)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China.

Wei Miao (W)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China.

Zhengjin Xu (Z)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China.

Fengcheng Li (F)

Key Laboratory of Crop Physiology, Ecology, Genetics and Breeding, Ministry of Agriculture, Shenyang Agricultural University, Shenyang, China. lifc_1983@163.com.

Classifications MeSH