Nutrient Deprivation

Nitrogen (N), sulfur (S) and phosphorous (P) deficiency limits plant growth and photosynthetic rates, which can cause a drastic decrease in crop productivity [1]. To study how photosynthetic organisms cope with nutrient limitation we use the model organism Chlamydomonas reinhardtii.

Chlamydomonas cells experiencing S deprivation exhibit a set of specific responses including the production of hydrolytic extracellular enzymes (arylsulfatases, ARS), alterations in cell wall structure (synthesis of new cell wall proteins, ECPs) [2], changes in the activities and composition of the photosynthetic apparatus [3], enhanced sulfate transport activity [4,5], increased scavenging of S from intracellular structures/molecules and the synthesis of enzymes required for efficient S assimilation [6]. The regulation of these responses involves a complex network of proteins and signal molecules that have been analyzed over the last 25 years. The generation of an insertional mutant library [7] has allowed identification of some of the main players depicted in Figure 1.

Figure 1Model depicting regulatory events associated with the acclimation of C. reinhardtii cells to S deprivation. For detailed description of this figure see [8]

In S-deprived cells there is no sulfate bound to SAC1 and the kinase SNRK2.2 is inhibited. Under these conditions the kinase SNRK2.1 is able to phosphorylate an unidentified transcription factor and induce a sequential, tiered genetic response. Firstly, sulfate transport activity is enhanced in a protein synthesis independent pathway. If this primary response is not enough to sustain the cells, the ARS73a protein participates in activation of second tier genes responsible for the late sulfur deprivation responses [8].

Recently, we have discovered a new phenomenon associated with the acclimation of cells to S deficiency. Late responses involving secretion of ARS and ECP proteins appears to require (or be facilitated by) a specific vacuole called the acidocalcisome [9] (Figure 2). These vacuoles are filled with polyphosphate, which complexes Ca2+ and Mg2+ and may have an important role in regulating the transcription of specific sulfur stress genes.

Figure 2. TEM Images of Chlamydomonas grown under nutrient replete and S deprivation conditions. Wild-type (21 gr), ars76 mutant and the complemented strain (C6-2) were grown in TAP medium with and without S [9]

Our latest work is focusing on the identification of new proteins and signaling molecules involved in the regulation of the responses described above.


[1] Marschner H. Mineral Nutrition of Higher Plants (1995) 2nd ed. Academic Press Limited, London. 

[2] Takahashi H, Braby CE and Grossman AR (2001) Sulfur economy and cell wall biosynthesis during sulfur     limitation of Chlamydomonas reinhardtii. Plant Physiol 127: 665-673.

[3] Zhang Z, Shrager J, Jain M, Chang CW, Vallon O and Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3: 1331-1348.

[4] Yildiz F, Davies JP and Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104: 981-987.

[5] Pootakham W and Grossman AR (2010) Identification and regulation of plasma membrane sulfate transporters in Chlamydomonas. Plant Physiol. 153: 1653-1658

[6] González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22: 1-27.

[7]  Pollock SV, Pootakham W, Shibagaki N, Moseley JL, Grossman AR (2005) Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosyn Res 86(3):475–489.

[8] Aksoy M, Pootakham W, Pollock SV, Moseley JL, Gonzalez-Ballester D, Grossman AR (2013) Tiered regulation of sulfur deprivation responses in Chlamydomonas reinhardtii and identification of an associated regulatory factor. Plant Physiol. 162(1):195-211.

[9] Aksoy M, Pootakham W, Grossman AR (2014) Critical function of a Chlamydomonas reinhardtii putative vacuolar transporter chaperone during nutrient deprivation. Plant Cell. 26(10):4214-4229.