Volatile Organic Compounds: A Bacterial Contribution to Plant Sulfur Nutrition

In the decade since it was first reported that volatile organic compounds (VOCs) released by bacteria can promote plant growth, it has become clear that VOC-mediated interactions between bacteria and plants are widespread (reviewed in Bailly and Weisskopf, 2012). The effects of VOCs on plants have been found to vary, ranging from plant growth promotion to inhibition, even within the same combination of plant and bacterial species. In addition, the mechanisms and ecological relevance of these interactions are not yet clear. Recently, Meldau et al. (2012) found that the B55 strain of the genus Bacillus isolated from Nicotiana attenuata (coyote tobacco) roots has strong plant growth promotion effects on wild-type N. attenuata and stronger effects on the ethylene-insensitive transgenic 35S-ethylene response1 (etr1) line, even increasing the survivorship of these ecologically impaired plants in the field. Now, Meldau et al. (pages 2731–2747) report that these effects are caused by Bacillus B55-released VOCs that contribute to N. attenuata sulfur (S) nutrition.

In their new work, Meldau et al. established that effects of B55 on N. attenuata were mediated by VOCs. They used bipartite Petri dishes in which the bacteria were grown separately from wild-type or 35S-etr1 seedlings. Seedlings of both genotypes grown in the presence of Bacillus B55 were larger, with more leaves, more lateral roots, and longer roots than those grown alone (see figure). These effects were larger in the 35S-etr1 overexpression line, which constitutively overproduces ethylene. Meldau et al. characterized the volatiles released by Bacillus B55, finding that dimethyl disulfide (DMDS) was present in large amounts in the headspace of Bacillus B55 grown alone but was much less abundant when Bacillus B55 was grown with wild-type N. attenuata seedlings. Further, treatment with pure DMDS in the headspace promoted the growth of the seedlings. This growth promotion was stronger in wild-type seedlings grown without SO₄^-2, suggesting that it is related to the S nutritional status of the plants.

Wild-type and 35S-etr1 N. attenuata seedlings grown for 12 d in the presence (bottom) of Bacillus B55 produce larger roots, with more lateral roots, than those grown without the bacteria (top) in the other portion of the Petri dish. (Reprinted from Meldau et al. [2013], Figure 1A.)

The authors tested whether the bacterial VOCs supply S to the seedlings. ³⁵S supplied in the medium on which the bacteria were grown was incorporated into seedling proteins. Because the only contact between the two sides of the Petri dish was through the headspace, this result strongly supports the idea that the seedlings absorbed volatile ³⁵S-labeled DMDS produced by Bacillus B55. Consistent with the stronger growth promotion of the transgenic line by Bacillus B55, the 35S-etr1 seedlings took up more ³⁵S than did wild type, especially when the seedlings were grown on medium containing SO₄^-2. Meldau et al. provide evidence that S metabolism is impaired in the 35S-etr1 line such that it requires more reduced S, possibly due to its constitutive production of ethylene.

Together, this work from Meldau et al. provides an explanation for the strong growth-promoting effect of Bacillus B55 on the 35S-etr1 N. attenuata line, i.e., that this line requires more reduced S than does the wild type and that the bacteria contribute to S nutrition in both lines. In revealing that VOCs from bacteria can contribute to the S nutrition of their associated plants, this report opens the door to a new area of study in terms of plant-microbe interactions, as well as revealing connections between ethylene and S metabolism.