Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Comparative analysis of the plastid conversion, photochemical activity and chlorophyll degradation in developing embryos of green-seeded and yellow-seeded pea (Pisum sativum) cultivars

Galina Smolikova https://orcid.org/0000-0001-5238-1851 A H , Olga Shiroglazova A , Galina Vinogradova B , Irina Leppyanen C , Ekaterina Dinastiya D E F , Olga Yakovleva G , Elena Dolgikh C , Galina Titova B , Andrej Frolov D F and Sergei Medvedev https://orcid.org/0000-0003-1127-1343 A
+ Author Affiliations
- Author Affiliations

A Department of Plant Physiology and Biochemistry, Saint Petersburg State University, Saint Petersburg, Russian Federation.

B Laboratory of Embryology and Reproductive Biology, Komarov Botanical Institute, Russian Academy of Sciences, Saint Petersburg, Russian Federation.

C Laboratory of Signal Regulation, All-Russia Research Institute for Agricultural Microbiology, Saint Petersburg, Russian Federation.

D Department of Biochemistry, Saint Petersburg State University, Saint Petersburg, Russian Federation.

E Postovsky Institute of Organic Synthesis, Ural Branch of Russian Academy of Sciences, Ekaterinburg, Russian Federation.

F Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Halle (Saale), Germany.

G Laboratory of Anatomy and Morphology, Komarov Botanical Institute, Russian Academy of Sciences, Saint Petersburg, Russian Federation.

H Corresponding author. Email: g.smolikova@spbu.ru

Functional Plant Biology 47(5) 409-424 https://doi.org/10.1071/FP19270
Submitted: 20 September 2019  Accepted: 8 December 2019   Published: 25 March 2020

Abstract

Developing seeds of some higher plants are photosynthetically active and contain chlorophylls (Chl), which are typically destroyed at the late stages of seed maturation. However, in some crop plant cultivars, degradation of embryonic Chl remains incomplete, and mature seeds preserve green colour, as it is known for green-seeded cultivars of pea (Pisum sativum L.). The residual Chl compromise seed quality and represent a severe challenge for farmers. Hence, comprehensive understanding of the molecular mechanisms, underlying incomplete Chl degradation is required for maintaining sustainable agriculture. Therefore, here we address dynamics of plastid conversion and photochemical activity alterations, accompanying degradation of Chl in embryos of yellow- and green-seeded cultivars Frisson and Rondo respectively. The yellow-seeded cultivar demonstrated higher rate of Chl degradation at later maturation stage, accompanied with termination of photochemical activity, seed dehydration and conversion of green plastids into amyloplasts. In agreement with this, expression of genes encoding enzymes of Chl degradation was lower in the green seeded cultivar, with the major differences in the levels of Chl b reductase (NYC1) and pheophytinase (PPH) transcripts. Thus, the difference between yellow and green seeds can be attributed to incomplete Chl degradation in the latter at the end of maturation period.

Additional keywords: chlorophylls, chloroplasts, embryogenesis, Pisum spp., photosynthesis, seed development.


References

Allen DK, Ohlrogge JB, Shachar-Hill Y (2009) The role of light in soybean seed filling metabolism. The Plant Journal 58, 220–234.
The role of light in soybean seed filling metabolism.Crossref | GoogleScholarGoogle Scholar | 19077167PubMed |

Allorent G, Osorio S, Ly Vu J, Falconet D, Jouhet J, Kuntz M, Fernie AR, Lerbs-Mache S, Macherel D, Courtois F, Finazzi G (2015) Adjustments of embryonic photosynthetic activity modulate seed fitness in Arabidopsis thaliana. New Phytologist 205, 707–719.
Adjustments of embryonic photosynthetic activity modulate seed fitness in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 25256557PubMed |

Alves-Carvalho S, Aubert G, Carrère S, Cruaud C, Brochot AL, Jacquin F, Klein A, Martin C, Boucherot K, Kreplak J, da Silva C, Moreau S, Gamas P, Wincker P, Gouzy J, Burstin J (2015) Full-length de novo assembly of RNA-seq data in pea (Pisum sativum L.) provides a gene expression atlas and gives insights into root nodulation in this species. The Plant Journal 84, 1–19.
Full-length de novo assembly of RNA-seq data in pea (Pisum sativum L.) provides a gene expression atlas and gives insights into root nodulation in this species.Crossref | GoogleScholarGoogle Scholar | 26296678PubMed |

Armstead I, Donnison I, Aubry S, Harper J, Hortensteiner S, James C, Mani J, Moffet M, Ougham H, Roberts L, Thomas A, Weeden N, Thomas H, King I (2007) Cross-species identification of Mendel’s I locus. Science 315, 73
Cross-species identification of Mendel’s I locus.Crossref | GoogleScholarGoogle Scholar | 17204643PubMed |

Baud S, Lepiniec L (2010) Physiological and developmental regulation of seed oil production. Progress in Lipid Research 49, 235–249.
Physiological and developmental regulation of seed oil production.Crossref | GoogleScholarGoogle Scholar | 20102727PubMed |

Borisjuk L, Rolletschek H (2009) The oxygen status of the developing seed. New Phytologist 182, 17–30.
The oxygen status of the developing seed.Crossref | GoogleScholarGoogle Scholar | 19207684PubMed |

Borisjuk L, Rolletschek H, Walenta S, Panitz R, Wobus U, Weber H (2003) Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity. The Plant Journal 36, 318–329.
Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity.Crossref | GoogleScholarGoogle Scholar | 14617089PubMed |

Borisjuk L, Nguyen TH, Neuberger T, Rutten T, Tschiersch H, Claus B, Feussner I, Webb AG, Jakob P, Weber H, Wobus U, Rolletschek H (2005) Gradients of lipid storage, photosynthesis and plastid differentiation in developing soybean seeds. New Phytologist 167, 761–776.
Gradients of lipid storage, photosynthesis and plastid differentiation in developing soybean seeds.Crossref | GoogleScholarGoogle Scholar | 16101913PubMed |

Borisjuk L, Neuberger T, Schwender J, Heinzel N, Sunderhaus S, Fuchs J, Hay JO, Tschiersch H, Braun H-P, Denolf P, Lambert B, Jakob PM, Rolletschek H (2013) Seed architecture shapes embryo metabolism in oilseed rape. The Plant Cell 25, 1625–1640.
Seed architecture shapes embryo metabolism in oilseed rape.Crossref | GoogleScholarGoogle Scholar | 23709628PubMed |

Bréhélin C, Kessler F (2008) Review the plastoglobule: a bag full of lipid biochemistry tricks. Photochemistry and Photobiology 84, 1388–1394.
Review the plastoglobule: a bag full of lipid biochemistry tricks.Crossref | GoogleScholarGoogle Scholar | 19067960PubMed |

Chen J, Ren G, Kuai B (2016) The mystery of Mendel’s stay-green: magnesium stays chelated in chlorophylls. Molecular Plant 9, 1556–1558.
The mystery of Mendel’s stay-green: magnesium stays chelated in chlorophylls.Crossref | GoogleScholarGoogle Scholar | 27867106PubMed |

Chung DW, Pružinská A, Hörtensteiner S, Ort DR (2006) The role of pheophorbide a oxygenase expression and activity in the canola green seed problem. Plant Physiology 142, 88–97.
The role of pheophorbide a oxygenase expression and activity in the canola green seed problem.Crossref | GoogleScholarGoogle Scholar | 16844830PubMed |

Clerkx EJM, Vries HB, Ruys GJ, Groot SPC, Koornneef M (2003) Characterization of green seed, an Enhancer of abi3-1 in Arabidopsis that affects seed longevity. Plant Physiology 132, 1077–1084.
Characterization of green seed, an Enhancer of abi3-1 in Arabidopsis that affects seed longevity.Crossref | GoogleScholarGoogle Scholar |

Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, Northey JGB, McCourt P, Samuel MA (2013) ABI3 controls embryo degreening through Mendel’s I locus. Proceedings of the National Academy of Sciences of the United States of America 110, 201308114

Diosady LL (2005) Chlorophyll removal from edible oils. International Journal of Applied Science and Engineering 3, 81–88.

Gaude N, Bréhélin C, Tischendorf G, Kessler F, Dörmann P (2007) Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. The Plant Journal 49, 729–739.
Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters.Crossref | GoogleScholarGoogle Scholar | 17270009PubMed |

Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |

Heinz Walz GmbH (2008) ‘PAM-2500 portable chlorophyll fluorometer: handbook of operation.’ (Heinz Walz GmbH: Effeltrich, Germany)

Hörtensteiner S (2013) Update on the biochemistry of chlorophyll breakdown. Plant Molecular Biology 82, 505–517.
Update on the biochemistry of chlorophyll breakdown.Crossref | GoogleScholarGoogle Scholar | 22790503PubMed |

Jiao K, Li X, Guo W, Su S, Luo D (2017) High-throughput RNA-seq data analysis of the single nucleotide polymorphisms (SNPs) and zygomorphic flower development in pea (Pisum sativum L.). International Journal of Molecular Sciences 18, 2710
High-throughput RNA-seq data analysis of the single nucleotide polymorphisms (SNPs) and zygomorphic flower development in pea (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar |

Kerr SC, Gaiti F, Beveridge CA, Tanurdzic M (2017) De novo transcriptome assembly reveals high transcriptional complexity in Pisum sativum axillary buds and shows rapid changes in expression of diurnally regulated genes. BMC Genomics 18, 221
De novo transcriptome assembly reveals high transcriptional complexity in Pisum sativum axillary buds and shows rapid changes in expression of diurnally regulated genes.Crossref | GoogleScholarGoogle Scholar | 28253862PubMed |

Kremnev D, Strand à (2014) Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis. Frontiers in Plant Science 5,
Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25161659PubMed |

Kusaba M, Tanaka A, Tanaka R (2013) Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence. Photosynthesis Research 117, 221–234.
Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence.Crossref | GoogleScholarGoogle Scholar | 23771643PubMed |

Leprince O, Pellizzaro A, Berriri S, Buitink J (2017) Late seed maturation: drying without dying. Journal of Experimental Botany 68, 827–841.

Li Z, Wu S, Chen J, Wang X, Gao J, Ren G, Kuai B (2017) NYEs/SGRs-mediated chlorophyll degradation is critical for detoxification during seed maturation in Arabidopsis. The Plant Journal 92, 650–661.
NYEs/SGRs-mediated chlorophyll degradation is critical for detoxification during seed maturation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28873256PubMed |

Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11, 591–592.
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.Crossref | GoogleScholarGoogle Scholar |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Meguro M, Ito H, Takabayashi A, Tanaka R, Tanaka A (2011) Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. The Plant Cell 23, 3442–3453.
Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 21934147PubMed |

Mornkham T, Wangsomnuk P, Fu Y-B, Wangsomnuk P, Jogloy S, Patanothai A (2013) Extractions of high quality RNA from the seeds of Jerusalem artichoke and other plant species with high levels of starch and lipid. Plants 2, 302–316.
Extractions of high quality RNA from the seeds of Jerusalem artichoke and other plant species with high levels of starch and lipid.Crossref | GoogleScholarGoogle Scholar | 27137377PubMed |

Nambara E, Okamoto M, Tatematsu K, Yano R, Seo M, Kamiya Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Science Research 20, 55–67.
Abscisic acid and the control of seed dormancy and germination.Crossref | GoogleScholarGoogle Scholar |

Onyilagha JC, Elliott BH, Buckner E, Okiror SO, Raney PJ (2011) Seed chlorophyll influences vigor in oilseed rape (Brassica napus L. var AC Excel.). The Journal of Agricultural Science 3, 73–79.

Pralon T, Kessler F (2016) Plastoglobules: lipid droplets at the thylakoid membrane. In ‘Chloroplasts Current Research and Future Trends’. pp. 171–186. (Caister Academic Press: Norfolk, UK)

Pružinská A, Anders I, Aubry S, Schenk N, Tapernoux-Luthi E, Muller T, Krautler B, Hortensteiner S (2007) In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. The Plant Cell 19, 369–387.
In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown.Crossref | GoogleScholarGoogle Scholar | 17237353PubMed |

Puthur JT, Shackira M, Saradhi PP, Bartels D (2013) Chloroembryos: a unique photosynthesis system. Journal of Plant Physiology 170, 1131–1138.
Chloroembryos: a unique photosynthesis system.Crossref | GoogleScholarGoogle Scholar | 23706538PubMed |

Roscoe TT, Guilleminot J, Bessoule J-J, Berger F, Devic M (2015) Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant & Cell Physiology 56, 1215–1228.
Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Ruuska SA, Schwender J, Ohlrogge JB (2004) The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes 1. Plant Physiology 136, 2700–2709.
The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes 1.Crossref | GoogleScholarGoogle Scholar | 15347783PubMed |

Saito GY, Chang YC, Wallings LL, Thomson WW (1989) A correlation in plastid development and cytoplasmic ultrastructure with nuclear gene expression during seed ripening in soybean. New Phytologist 113, 459–469.
A correlation in plastid development and cytoplasmic ultrastructure with nuclear gene expression during seed ripening in soybean.Crossref | GoogleScholarGoogle Scholar |

Sakuraba Y, Park S-Y, Kim Y-S, Wang S-H, Yoo S-C, Hörtensteiner S, Paek N-C (2014) Arabidopsis STAY-GREEN2 is a negative regulator of chlorophyll degradation during leaf senescence. Molecular Plant 7, 1288–1302.
Arabidopsis STAY-GREEN2 is a negative regulator of chlorophyll degradation during leaf senescence.Crossref | GoogleScholarGoogle Scholar | 24719469PubMed |

Sakuraba Y, Park S-Y, Paek N-C (2015) The divergent roles of STAYGREEN (SGR) homologs in chlorophyll degradation. Molecules and Cells 38, 390–395.
The divergent roles of STAYGREEN (SGR) homologs in chlorophyll degradation.Crossref | GoogleScholarGoogle Scholar | 25913011PubMed |

Sakuraba Y, Han S-H, Lee S-H, Hörtensteiner S, Paek N-C (2016) Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription. Plant Cell Reports 35, 155–166.
Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription.Crossref | GoogleScholarGoogle Scholar | 26441053PubMed |

Sato Y, Morita R, Nishimura M, Yamaguchi H, Kusaba M (2007) Mendel’s green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proceedings of the National Academy of Sciences of the United States of America 104, 14169–14174.
Mendel’s green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway.Crossref | GoogleScholarGoogle Scholar | 17709752PubMed |

Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M (2009) Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. The Plant Journal 57, 120–131.
Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice.Crossref | GoogleScholarGoogle Scholar | 18778405PubMed |

Shimoda Y, Ito H, Tanaka A (2016) Arabidopsis STAY-GREEN, Mendel’s green cotyledon gene, encodes magnesium-dechelatase. The Plant Cell 28, 2147–2160.
Arabidopsis STAY-GREEN, Mendel’s green cotyledon gene, encodes magnesium-dechelatase.Crossref | GoogleScholarGoogle Scholar | 27604697PubMed |

Smolikova GN, Medvedev SS (2015) Seed carotenoids: synthesis, diversity, and functions. Russian Journal of Plant Physiology 62, 1–13.
Seed carotenoids: synthesis, diversity, and functions.Crossref | GoogleScholarGoogle Scholar |

Smolikova GN, Medvedev SS (2016) Photosynthesis in the seeds of chloroembryophytes. Russian Journal of Plant Physiology 63, 1–12.
Photosynthesis in the seeds of chloroembryophytes.Crossref | GoogleScholarGoogle Scholar |

Smolikova GN, Laman NA, Boriskevich OV (2011) Role of chlorophylls and carotenoids in seed tolerance to abiotic stressors. Russian Journal of Plant Physiology 58, 965–973.
Role of chlorophylls and carotenoids in seed tolerance to abiotic stressors.Crossref | GoogleScholarGoogle Scholar |

Smolikova GN, Shavarda AL, Alekseichuk IV, Chantseva VV, Medvedev SS (2016) The metabolomic approach to the assessment of cultivar specificity of Brassica napus L. seeds. Russian Journal of Genetics: Applied Research 6, 78–83.
The metabolomic approach to the assessment of cultivar specificity of Brassica napus L. seeds.Crossref | GoogleScholarGoogle Scholar |

Smolikova G, Dolgikh E, Vikhnina M, Frolov A, Medvedev S (2017) Genetic and hormonal regulation of chlorophyll degradation during maturation of seeds with green embryos. International Journal of Molecular Sciences 18, 1993
Genetic and hormonal regulation of chlorophyll degradation during maturation of seeds with green embryos.Crossref | GoogleScholarGoogle Scholar |

Smolikova G, Kreslavski V, Shiroglazova O, Bilova T, Sharova E, Frolov A, Medvedev S (2018) Photochemical activity changes accompanying the embryogenesis of pea (Pisum sativum) with yellow and green cotyledons. Functional Plant Biology 45, 228
Photochemical activity changes accompanying the embryogenesis of pea (Pisum sativum) with yellow and green cotyledons.Crossref | GoogleScholarGoogle Scholar |

Teixeira RN, Ligterink W, França-Neto J de B, Hilhorst HWM, da Silva EAA (2016) Gene expression profiling of the green seed problem in soybean. BMC Plant Biology 16, 37
Gene expression profiling of the green seed problem in soybean.Crossref | GoogleScholarGoogle Scholar | 26829931PubMed |

Thomas H, Ougham H (2014) The stay-green trait. Journal of Experimental Botany 65, 3889–3900.
The stay-green trait.Crossref | GoogleScholarGoogle Scholar | 24600017PubMed |

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |

Tschiersch H, Borisjuk L, Rutten T, Rolletschek H (2011) Gradients of seed photosynthesis and its role for oxygen balancing. Bio Systems 103, 302–308.
Gradients of seed photosynthesis and its role for oxygen balancing.Crossref | GoogleScholarGoogle Scholar | 20837098PubMed |

van Wijk KJ, Kessler F (2017) Plastoglobuli: plastid microcompartments with integrated functions in metabolism, plastid developmental transitions, and environmental adaptation. Annual Review of Plant Biology 68, 253–289.
Plastoglobuli: plastid microcompartments with integrated functions in metabolism, plastid developmental transitions, and environmental adaptation.Crossref | GoogleScholarGoogle Scholar | 28125283PubMed |

Zinsmeister J, Lalanne D, Terrasson E, Chatelain E, Vandecasteele C, Vu BL, Dubois-Laurent C, Geoffriau E, Le Signor C, Dalmais M, Gutbrod K, Dörmann P, Gallardo K, Bendahmane A, Buitink J, Leprince O (2016) ABI5 is a regulator of seed maturation and longevity in legumes. The Plant Cell 28, 2735–2754.
ABI5 is a regulator of seed maturation and longevity in legumes.Crossref | GoogleScholarGoogle Scholar | 27956585PubMed |

Zhukov VA, Zhernakov AI, Kulaeva OA, Ershov NI, Borisov AY, Tikhonovich IA (2015) De novo assembly of the pea (Pisum sativum L.) nodule transcriptome. International Journal of Genomics 2015, 695947
De novo assembly of the pea (Pisum sativum L.) nodule transcriptome.Crossref | GoogleScholarGoogle Scholar | 26688806PubMed |