Responses to Macronutrient Deprivation

  • Arthur R. Grossman
  • David Gonzalez-Ballester
  • Nakako Shibagaki
  • Wirulda Pootakham
  • Jeffrey Moseley


Photosynthetic organisms have developed elaborate mechanisms to acquire macronutrients and to adjust to conditions in which those nutrients become limiting to growth. Some of the responses of photosynthetic organisms to macronutrient limitation may be specific for a particular nutrient and involve the development of various mechanisms to scavenge the limiting nutrient from the external milieu, which may require elevated synthesis of high affinity transport systems, the redistribution of internal nutrient stores and the synthesis of hydrolytic enzymes that release the nutrient from organic substrates in the soil. Other responses may be of a more general nature, occurring during a number of different nutrient limitation conditions, and involve modifying the biosynthetic machinery of the cell, including the photosynthetic apparatus. In this review we focus on the acquisition of the macronutrients nitrogen, sulfur and phosphorus from the environment, and the ways in which the unicellular green alga Chlamydomonas reinhardtii acclimates to changes in its nutrient environment.


ammonium assimilation macronutrients nitrate nutrient deprivation phosphate phosphorus sulfur transport 



Arabiopsis amino acid permease

ABC transporter

ATP binding cassette transporter


adenosine monophosphate


ammonium transporter


gene encoding a protein that confers resistance to paromomycin


adenosine 5′-phosphosulfate kinase


adenosine 5′-phosphosulfate reductase


adenosine 5′-phosphosulfate


gene encoding an enzyme in the pathway for arginine biosynthesis(argininosuccinate lyase)




mutant in a serine threonine kinase associated with control of the responses of Chlamydomonas reinhardtii to sulfur deprivation


gene encoding O-acetylserine (thiol) lyase




gene encoding ATP sulfurylase


chloroplast DNA


chloroplast RNA


membrane component of ABC transporter for sulfate




dimethyl sulfonio-proprionate


chloride/bicarbonate antiporter


extracellular polypeptide


expressed sequence tag


regulatory locus involved in the utilization of nitrogen in Chlamydomonas reinhardtii






glutamine-2-oxoglutarate amino-transferase


glutamine synthetase




high affinity nitrite transporter


high affinity nitrate transporter


high fluorescence mutant deficient for sulfolipids


hydrogenase proteins


inosine monophosphate

IRL protein

isoflavone reductase-like protein in maize that has few sulfur amino acids


low affinity nitrate transporter


light harvesting complex


light harvesting complex protein, stress related


lysine histidine transporter

LOV domain

domain that can be involved in sensing light, oxygen and voltage


low phosphate bleaching phenotype

MYB domain

derived from myeloblastosis and often in regulatory proteins


nitrite-nitrate transporter genes


nitrate reductase gene


nitrite reductase gene


nitrate assimilation/regulation loci in Chlamydomonas reinhardtii


nitrite reductase


nitrate reductase


regulatory locus involved in the utilization of nitrogen in Chlamydomonas reinhardtii


nitrate transporter genes




O-acetylserine (thiol) lyase




3′-phosphoadenosine 5′-phosphosulfate

PAS domain

protein domain involved in sensing and protein-protein interaction named from Per (period circadian protein), Arnt (Ah receptor nuclear translocator protein) and Sim (single-minded protein)








phosphate regulatory E2 ubiquitin conjugase


protein associated with extracellular phosphatase activity in Chlamydomonas reinhardtii and Volvox carteri


involved in phosphorus deprivation responses in Arabidopsis thaliana


inorganic phosphate




polynucleotide Phosphate


polynucleotide phosphorylase


plastoquinone pool


phosphate transporter, type A class


phosphate transporter, type B class

QA and QB

primary and secondary acceptors of photosystem II, respectively


rhesus protein


reactive oxygen species


regulator in Chlamydomonase reinhardtii associated with phosphate stress response




nucleotide binding protein of ABC type transporter


transporter-like proteins associated with control of the responses of Chlamydomonas reinhardtii to sulfur deprivation


mutant in the gene encoding SAC1


serine threonine kinase associated with control of the responses of Chlamydomonas reinhardtii to sulfur deprivation


mutant in the gene encoding SAC3




serine acetyltransferase


selenenium binding protein


substrate binding protein of ABC type transporter


gene encoding serine acetyltransferase


ubiquitiin ligase similar to Skp1-Cullin-F-box protein (SCF) ubiquitin ligases


sulfite reductase


sap interacting zinc finger protein which is plant SUMO E3 ligase


family of anion transporters that include the sulfate transporters


sulfate transporter (animal type)


SNF-related kinase


antisigma factor antagonist in Bacillus subitilis with similarity to STAS domain


UDP-sulfoquinovose synthase


mutant in the gene encoding SQD1




domain found attached to certain anion transporters such as the sulfate transporter that has homology to an antisigma factor antagonist in Bacillus subtilis; sulfate transporter and sigma factor domain


sulfate transporter in yeast


component of chloroplast sulfate transporter in Chlamydomonas reinhardtii


sulfate transporters (plant type)


small ubiquitin-like modifier


trans-membrane domain


domain of unknown function found associated with some transporters


uridine diphosphate


vacuolar transport chaperone


5-bromo-4-chloro-3-indolyl sulfate



Some of this work was supported by United States Department of Agriculture grant 2002-35301-12178 and National Science Foundation grants MCB 0235878 and MCB 0824469, all awarded to A.R.G. David Gonzalez Ballester was supported by the Ministerio de Educación y Ciencia (Spain).


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Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Arthur R. Grossman
    • 1
  • David Gonzalez-Ballester
    • 1
  • Nakako Shibagaki
    • 1
  • Wirulda Pootakham
    • 1
    • 2
  • Jeffrey Moseley
    • 1
  1. 1.Department of Plant BiologyThe Carnegie InstitutionStanfordUSA
  2. 2.Department of Biological SciencesStanford UniversityStanfordUSA

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