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

Photochemical activity changes accompanying the embryogenesis of pea (Pisum sativum) with yellow and green cotyledons

Galina Smolikova A E , Vladimir Kreslavski B C , Olga Shiroglazova A , Tatiana Bilova A , Elena Sharova A , Andrej Frolov D and Sergei Medvedev A E
+ Author Affiliations
- Author Affiliations

A Department of Plant Physiology and Biochemistry, Saint-Petersburg State University, 7/9 Universitetskaya nab., St. Petersburg 199034, Russia.

B Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow 127276, Russia.

C Institute of Basic Biological Problems, Russian Academy of Sciences, Institutskaya Street 2, Pushchino, Moscow Region 142290, Russia.

D Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Weinberg 3, Halle (Saale) 06120, Germany.

E Corresponding authors. Emails: g.smolikova@spbu.ru; s.medvedev@spbu.ru

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 1923 June 2016.

Functional Plant Biology 45(2) 228-235 https://doi.org/10.1071/FP16379
Submitted: 9 November 2016  Accepted: 18 February 2017   Published: 29 March 2017

Abstract

The pea seeds are photosynthetically active until the end of the maturation phase, when the embryonic chlorophylls degrade. However, in some cultivars, the underlying mechanisms are compromised, and the mature seeds preserve green colour. The residual chlorophylls can enhance oxidative degradation of reserve biomolecules, and affect thereby the quality, shelf life and nutritive value of seeds. Despite this, the formation, degradation, and physical properties of the seed chlorophylls are still not completely characterised. So here we address the dynamics of seed photochemical activity in the yellow- and green-seeded pea cultivars by the pulse amplitude modulation (PAM) fluorometric analysis. The experiments revealed the maximal photochemical activity at the early- and mid-cotyledon stages. Thereby, the active centres of PSII were saturated at the light intensity of 15–20 µmol photons m–2 s–1. Despite of their shielding from the light by the pod wall and seed coat, photochemical reactions can be registered in the seeds with green embryo. Importantly, even at the low light intensities, the photochemical activity in the coats and cotyledons could be detected. The fast transients of the chlorophyll a fluorescence revealed a higher photochemical activity in the coat of yellow-seeded cultivars in comparison to those with the green-seeded ones. However, it declined rapidly in all seeds at the late cotyledon stage, and was accompanied with the decrease of the seed water content. Thus, the termination of photosynthetic activity in seeds is triggered by their dehydration.

Additional keywords: chlorophyll, chlorophyll a fluorescence, embryogenesis, 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 | 1:CAS:528:DC%2BD1MXlsVWltb4%3D&md5=e5ec8bdf830816e5c7e6c20b82145babCAS |

Allorent G, Osorio S, Vu JL, 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 | 1:CAS:528:DC%2BC2cXitFansbfN&md5=1fb9cc8184fc9c5024895a32c69d5464CAS |

Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annual Review of Plant Physiology 37, 93–136.
Photoregulation of the composition, function, and structure of thylakoid membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xktl2gs74%3D&md5=0316b25a5b813e22abd706f3d234c661CAS |

Armstead I, Donnison I, Aubry S, Harper J, Hörtensteiner 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 locus. Science 315, 73
Cross-species identification of Mendel’s locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlGqtL3P&md5=3fa43e1dbec71c0d33623dbdfeed0f2dCAS |

Asokanthan PS, Johnson RW, Griffith M, Krol M (1997) The photosynthetic potential of canola embryos. Physiologia Plantarum 101, 353–360.
The photosynthetic potential of canola embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvVWmtb0%3D&md5=221ff1aa5ca8c5acaf4a71eb75ffdad6CAS |

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 | 1:CAS:528:DC%2BD1MXksVKhtb4%3D&md5=ff8e89267ac098359259ed2ffc57aea2CAS |

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 | 1:CAS:528:DC%2BD3sXpvVykurs%3D&md5=92a2d2571bd38f138fe138e16d1869f5CAS |

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 | 1:CAS:528:DC%2BD2MXhtVGitr7N&md5=740ff14b5293260e9b0776e8517a4201CAS |

Eastmond P, Kolacna L, Rawsthorne S (1996) Photosynthesis by developing embryos of oilseed rape (Brassica napus L.). Journal of Experimental Botany 47, 1763–1769.
Photosynthesis by developing embryos of oilseed rape (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsFOgsA%3D%3D&md5=f5d7bb46a4a9ea49efea994046de8b34CAS |

Genty B, Briantais JM, 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 | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=ca3f55cdd9fa28062542f823d0b95a3aCAS |

Georgieva K, Mihailova G (2016) Drought tolerance of photosynthesis. In ‘Handbook of photosynthesis’. (3rd edn) (Ed. M Pessarakli) pp. 683–696. (CRC Press: Boca Raton, FL, USA)

Hills MJ (2004) Control of storage-product synthesis in seeds. Current Opinion in Plant Biology 7, 302–308.
Control of storage-product synthesis in seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVamsL0%3D&md5=7b2b541623b414dc8eb534faa5ea7935CAS |

Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends in Plant Science 14, 155–162.
Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence.Crossref | GoogleScholarGoogle Scholar |

Johnson RW, Asokanthan PS, Griffith M (1997) Water and sucrose regulate canola embryo development. Physiologia Plantarum 101, 361–366.
Water and sucrose regulate canola embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvVWmtbo%3D&md5=a2af22f8802373824b7f96413d129782CAS |

Kulkarni MG, Dalai AK, Bakhshi NN (2006) Utilization of green seed canola oil for biodiesel production. Journal of Chemical Technology and Biotechnology 81, 1886–1893.
Utilization of green seed canola oil for biodiesel production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12htbjM&md5=f9667beb811b3e00e5021d089b9e1f0dCAS |

Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 11, 591–592.

Mendel G (1866) Versuche über Pflanzen-Hybriden Verh. Naturforsch. Verh Naturforsch Ver Brünn 4, 3–47.

Nakajima S, Ito H, Tanaka R, Tanaka A (2012) Chlorophyll b reductase plays an essential role in maturation and storability of Arabidopsis seeds. Plant Physiology 160, 261–273.
Chlorophyll b reductase plays an essential role in maturation and storability of Arabidopsis seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlOmtLzP&md5=e6d92aea3bd03f277b9cea1a94a8eeeaCAS |

Palanisamy K, Vivekanandan M (1986) Photosynthetic functions and induction of etiolation in chloroembryos of Dolichos lablab L. Journal of Plant Physiology 123, 395–399.
Photosynthetic functions and induction of etiolation in chloroembryos of Dolichos lablab L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XksFyisLk%3D&md5=3b0f406b819789210b29f33b5366042cCAS |

Pinfield NJ, Stobart AK, Crawford RM, Beckett A (1973) Carbon assimilation by sycamore cotyledons during early seedling development. Journal of Experimental Botany 24, 1203–1207.
Carbon assimilation by sycamore cotyledons during early seedling development.Crossref | GoogleScholarGoogle Scholar |

Porra RJ (2002) The checkered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research 73, 149–156.
The checkered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVGltb8%3D&md5=1df0752458c6141ec1300295824ae114CAS |

Puthur JT, Shackira AM, 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 | 1:CAS:528:DC%2BC3sXot1Oisbw%3D&md5=f7f6f18d1b2ef55978dbed0710d86cc7CAS |

Ruuska SA, Schwender J, Ohlrogge JB (2004) The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiology 136, 2700–2709.
The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOru7k%3D&md5=975699f81150477ef96d19126997d72fCAS |

Saito GY, Chang YC, Walling LL, Thompson 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 | 1:CAS:528:DyaK3cXhtlKjurg%3D&md5=1edf4c8fda1d1bf330a9a8adf77a04c9CAS |

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 | 1:CAS:528:DC%2BD1MXhtFOiu78%3D&md5=13ef77725d243ad97fadee729bf4c0b0CAS |

Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hörtensteiner S (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. The Plant Cell 21, 767–785.
Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFyltbg%3D&md5=e0ae430cf16a8949a4a6a3bb37b15ab2CAS |

Schwender J, Goffman F, Ohlrogge JB, Shachar-Hill Y (2004) Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432, 779–782.
Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVGmtLfJ&md5=8ed3512a59deb16570b53bd43737b5efCAS |

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 | 1:CAS:528:DC%2BC28XisFOks7c%3D&md5=9dc87223f404802daef72cf9ac4eb5caCAS |

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 | 1:CAS:528:DC%2BC3MXht12qs77M&md5=cbec0c9cd36461b28d8006c2ef4044f8CAS |

Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transients. In ‘Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration’. (Eds GC Papageorgiou, Govindjee) pp. 321–362. (Springer: Dordrecht, The Netherlands)

Suzuki T, Kunieda T, Murai F, Morioka S, Shioi Y (2005) Mg-dechelation activity in radish cotyledons with artificial and native substrates, Mg-chlorophyllin a and chlorophyllide a. Plant Physiology and Biochemistry 43, 459–464.
Mg-dechelation activity in radish cotyledons with artificial and native substrates, Mg-chlorophyllin a and chlorophyllide a.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFCksbc%3D&md5=6bb7419d04a18050927a99204ce97208CAS |

Toyoda KA (1961) Complementary note on the chlorophyll in some spermatophyte seeds. Botanical Magazine Tokyo 74, 310–312.
Complementary note on the chlorophyll in some spermatophyte seeds.Crossref | GoogleScholarGoogle Scholar |

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 | 1:CAS:528:DC%2BC3MXhtVSrsrc%3D&md5=1d1799cd6cc0665005e9a464d9ecd088CAS |

Weber H, Borisjuk L, Wobus U (2005) Molecular physiology of legume seed development. Annual Review of Plant Biology 56, 253–279.
Molecular physiology of legume seed development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVaru7k%3D&md5=05f1e86b591d0da185c82efc9c530d87CAS |

Willows RD (2004) Chlorophylls. In ‘Plant pigments and their manipulation’. (Ed. KM Davies) pp. 23–56. (CRC Press: Boca Raton, FL, USA)

Yakovlev MS (1969) Embryogenesis and some problems of phylogenesis. Rev. Cytol. Biol. Veg. 32, 325–330.

Yakovlev MS, Zhukova GY (1980) Chlorophyll in embryos of angiosperm seeds, a review. Botaniska Notiser 133, 323–336.

Zhang Y, Mulpuri S, Liu A (2016) High light exposure on seed coat increases lipid accumulation in seeds of castor bean (Ricinus communis L.), a non-green oilseed crop. Photosynthesis Research 128, 125–140.
High light exposure on seed coat increases lipid accumulation in seeds of castor bean (Ricinus communis L.), a non-green oilseed crop.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVyqtrnL&md5=84ab894bbcff0c2f990e00ab63219547CAS |